Neuroscience Vol. 60, No. 3, pp.

587-605, 1994
Elsevier Science Ltd
IBRO
Pergamon 0306-4522(94)E0008-R Printed in Great Britain
0306-4522/94 $7.00 + 0.00

COMMENTARY

THE BRAIN AS A DYNAMIC PHYSICAL SYSTEM

T. M. MCKENNA,*~ T. A. MCMULLEN? and M. F. SHLESINGER~

TDivision of Cognitive and Neural Sciences and IDivision of Physics, Office of Naval Research,
Arlington, VA 22217, U.S.A.

Abstract-The brain is a dynamic system that is non-linear at multiple levels of analysis. Characterization
of its non-linear dynamics is fundamental to our understanding of brain function. Identifying families of
attractors in phase space analysis, an approach which has proven valuable in describing non-linear
mechanical and electrical systems, can prove valuable in describing a range of behaviors and associated
neural activity including sensory and motor repertoires. Additionally, transitions between attractors may
serve as useful descriptors for analysing state changes in neurons and neural ensembles.
Recent observations of synchronous neural activity, and the emerging capability to record the
spatiotemporal dynamics of neural activity by voltage-sensitive dyes and electrode arrays, provide
opportunities for observing the population dynamics of neural ensembles within a dynamic systems
context. New developments in the experimental physics of complex systems, such as the control of chaotic
systems, selection of attractors, attractor switching and transient states, can be a source of powerful new
analytical tools and insights into the dynamics of neural systems.

CONTENTS
1. Introduction 587
2. Single neuron dynamics 588
3. Transitions between dynamic states: driving parameters 590
4. Transitions produced by graded inputs 591
5. Perturbation-induced transitions 592
6. Noise-induced transitions 592
7. Neural ensemble dynamics at the mesoscale 594
8. Intermittent synchronized oscillations 594
9. Spatiotemporal modes of activity in the brain 598
IO. Coupled non-linear oscillators in motor control: chains of oscillators 600
11. Mammalian olivocerebellar system as a two-dimensional isochronous sheet of
coupled oscillators 601
12. Conclusions 602
References

1. INTRODUCTION system is rich with complex, non-linear dynamic

behavior. From single neuron burst patterns to global
Until recently, physics lacked the tools to contribute electroencephalogram (EEG) measures, phase space
to the analysis of complex biological systems. Physics descriptors have revealed a wide range of non-linear
has traditionally focused on the very large, the very dynamic phenomena. While earlier neural models
small and, in general, the very simple physical sys- incorporated non-linear equations and attempts were
tems. However, the recent emergence of a physics made to account for non-linear behavior in exper-
of complex systems which explicitly considers non- imental data (cf. Refs 10, 22, 27, 37, 72 and 97), in
linear, non-equilibrium, non-stationary, open and the last decade there have been a number of advances
strongly coupled systems has provided a new oppor- in the understanding of the rich behaviors of non-
tunity for neuroscience to pursue the analysis of the linear systems, including many complex behaviors
brain as a dynamic physical system. This is a timely which only became apparent with the widespread
development, since current neuroscience has provided use of high performance computers. These newer
abundant evidence that, at all levels, the nervous developments may give important insights into the
behavior of complex living systems, including neural
*To whom correspondence should be addressed at: ONR systems.
Code 342 CN, 800 N. Quincy Street, Arlington, VA We will review the evidence on non-linear dynamic
222 17-5660, U.S.A.
system behavior in neural systems, including the
Abbreviations: EEG, electroencephalogram: IO, inferior
olive; MEG, magnetoencephalogram; RF, receptor field; single neuron level, neural ensembles in sensory and
SR, stochastic resonance. motor systems, and spatiotemporal modes of activity

587
588 T. M. MCKENNA et al.

in large neural ensembles. In addition to recounting a periodically driven non-linear system possesses
these significant new results, we hope to provide the a strange chaotic attractor, and the same system
neuroscience reader with a glimpse of the tremendous when driven quasi-periodically possesses a strange
potential for dynamic systems theory in under- non-chaotic attractor (quasi-periodic means driven
standing the sequential changes in system dynamics by two incommensurate frequencies). When a dy-
underlying sensorimotor behavior. Just as physical namic system exhibits a strange attractor, it also
systems can be characterized as evolving across exhibits high sensitivity to initial conditions. Identify-
different regimes (periodic, quasi-periodic, chaotic, ing attractors in phase space is not the end goal of
etc.) under the control of one or more system par- neural dynamics; however, they provide the building
ameters, neurons and neural ensembles also pass blocks for describing much more complex system
through a repertoire of regimes under the control behavior. For example, in the domain of the
of driving inputs such as precisely timed synaptic physics of complex systems (see Vohra et LZ~.~~), small
inputs. An important physical property playing a changes in the conditions in systems operating in a
critical role in such state transitions is noise, and we very non-linear fashion, near instabilities, can change
will review two new concepts on the role of noise attractors to repellers, change fixed points from
in neural systems. Most man-made systems, and stable to unstable, make attractors collide, and create,
engineering paradigms that have spawned many of destroy, modify or reverse the sequence of changes
the analogies that guide neural models (batteries, in phase space. These changes can be used to
electric power grid, telephone switchboard, servo- detect, control and synchronize signals in physical
control, electronic circuits, digital computers), are systems, and they provide a rich repertoire for
designed to be stable. By contrast, we advance the describing the dynamics of neural systems. Another
hypothesis that real neural systems operate near advantage of describing neural activity in terms of
instability, and this confers the ability to respond attractors in phase space is that it may permit the use
rapidly and with a large flexible repertoire of sensory of the same descriptors at different levels of organiz-
and motor patterns. ation of the nervous system, e.g. single neurons and
It is helpful to define the terms used in character- neural ensemble activity, and permits comparison
izing dynamic systems. The “phase space” of a across sensory and motor systems as well as across
dynamic system is a mathematical space with inde- species. Phase space descriptors help to identify
pendent co-ordinates representing the dynamic vari- dynamic patterns in data that are not obvious
ables needed to specify the instantaneous state of the in traditional physiological measurements. The
system.4.65 A common example in mechanical systems examples we will present are meant to be illustrative,
would be a plot of position vs velocity. In the case of rather than definitive, for these pioneering studies are
neural activity, one might plot two or more measur- at the beginning of a long series of investigations that
able variables. A “phase space embedding” is a type will likely produce far more sophisticated dynamic
of multidimensional phase plot which represents the descriptors of neural systems as the full range of neural
relations among F(t), F(t + At), F(t + 281) where phenomena are considered.
F(t) is a measurable variable (e.g. voltage) at time t
and A\t is an appropriate lag. This is particularly 2. SINGLE NEURON DYNAMICS
useful with experimental neural data, where it is much
easier to obtain measures of a single variable at many Currently, the best characterized neurons, in terms
times, but it may be difficult to directly measure other of dynamic analysis, are the invertebrate bursting
system parameters which reflect independent degrees neurons. In both experimental and modeling analy-
of freedom. An “attractor” is a trajectory or point in ses, evidence has emerged that these neurons exhibit
phase space to which the system will converge from chaotic attractors in phase space.‘6~‘7~20@~70Mpistos
a set of initial co-ordinates. A non-linear system may et a1.6*.69analysed the bursting pattern in motorneu-
have more than one attractor. One important rons in the sea slug Pleurobranchea. The time series
example of an attractor is the limit cycle. We will derived from the envelopes of the high frequency
discuss limit cycles in relation to central pattern bursts of these neurons exhibited the sign of strange
generators for motor control. chaotic attractors: a positive Lyapunov exponent.
One can measure the average rate at which In addition, low correlation dimensions were calcu-
neighboring trajectories on an attractor diverge in a lated, which is consistent with clear structure in the
phase plot via a rate called the “Lyapunov expo- Poincare plots. [For a time series one can calculate
nent”. If it is negative, orbits of the trajectory tend how many points N(E) are within E in value of
to converge and the orbit is stable. If the Lyapunov a chosen point. The manner in which this varies
exponent is positive for at least one degree of free- with E determines the “correlation dimension” d, as
dom, adjacent orbits diverge exponentially in time, N(E) E Ed, as E tends to zero.] “Poincare plots” or
and the orbit is “chaotic”. If the attractor for “sections” are slices cut through the phase space
the orbit is fractal, then the attractor is called a embedding plots. An example is shown in Fig. 1.68
“strange attractor”. Strange attractors without At the top is the low-pass filtered burst pattern of
chaotic orbits also exist. Several examples exist where a single neuron. Below it is a 2-D phase space
 Non-linear dynamics of neural systems 589

Bursting Pattern from Invertebrate Neuron

l!.,.,
0 25 50
‘I
75
I 8.1,
100 125
c
150
‘1 175
Time Ls)

Phase Space Embedding PoincarCtSection

0.8 w3
f.0
f. -6
0.6
r 0.0 7
SO.4 6.
s
‘0
-1.
0.2
0

-2. 0.0 ~
0-2 -1 0 f 2 0.0 0.2 0.4 0.6 0.8 1.0

f (0 tn

Fig. I. Phase space analysis of the bursting pattern of a motor neuron from the mollusc P~e~~o~r~chea
during a bout of the bite-swallow motor pattern. Top: frequency of discharge of the neuron (reciprocal
of interspike intervaIs). Bottom left: 2-D phase portrait of band-pass filtered version of frequency plot
at top. A Poincare section was taken at the horizontal line. Bottom right: Poincare section or map of return
times as a function of preceding return time, constructed by plotting the successive times at which
trajectories pass in the same direction through the horizontal line. The numbers next to each point indicate
the sequence of ordered pairs. After Mpistos et a1.68.69

embedding, and a Poincare section of the embedding,
taken from the indicated slice through the em-
bedding. Each 360” turn of the trajectory in the phase
embedding corresponds to a burst of the neuron. In
the Poincare section, points show the return time
where the trajectories cross the 1-D section, and the
time ordered sequence of numbered points charac-
terize the system dynamics. In a later section we will
show how physicists use real-time Poincare plots to
track and control the dynamics of physical systems
and isolated hearts.
What is the significance of chaotic-like bursting to
the organism? In this case, Mpistos et a1.69,70
speculate
that the chaotic and variable activity of neurons
could provide a route for pattern switching in the
neural ensemble. The sensitivity to initial conditions
leads to the blending of several behavioral responses
in the presence of disparate cues which alone
elicit different responses, via a self-organizing co-
operativity within an ensemble, as well as providing
a history and context sensitivity to the ensemble.
Recently, Byrne and his associates’6 demonstrated
seven different attractors in the bursting pattern of
model ApZysiu R15 neurons in realistic simulations.
These model neurons show seven different modes of
bursting. In phase plane plots of the two most slowfy
changing parameters during the bursts of model
neuron (internal Ca2+ and activation of a slow
inward current), seven separate attractors are
revealed (Fig, 2). Some of these attractors are limit
cycles, and some are strange chaotic attractors. In
the simulations, the neuron will remain in one attrac-
tor (for many thousands of orbits) until a synaptic
input is applied at a particular phase of the burst,
then the neuron shifts to another attractor. This
result raises a number of issues. First, under what
conditions and by what means does the organism use
this attractor switching? Is this used for multiplexing
in neuron-sparse invertebrate circuits? Is there an
equivalent m~hanism in vertebrates? The ability of
perturbations to switch dynamic modes in a phase-
sensitive manner brings us to the general issue of how
590 T. M. MCKENNA rt al.

.6 -

I I I I
250 300 350 400 4!
Internal Free Calcium Concentration (nM)

Fig. 2. Phase plane projection of dynamic activity of a model of the R15 neuron from the mollusc Aplysiu.
The values of two model quantities, activation of a slow inward current and internal calcium
concentration, were plotted for each attractor for 200 s of simulation time, after 6 h of simulated time had
elapsed to assure steady state activity. The different trajectories correspond to distinct discharge patterns
produced by different initial values of the state variables. I, Bursting limit cycle; II, outer chaotic attractor;
III-V, limit cycle; VI, chaotic attractor; VII, beating limit cycle. After Canavier er al.”

complex systems move through multiple dynamic chaos in which several simultaneous independent
states. frequencies appear before the chaotic regime is
entered. These routes have not been demonstrated
in neural systems, nor adequately investigated.
3. TRANSITIONS BETWEEN DYNAMIC STATES:
DRIVING PARAMETERS Additionally, chaotic crises and transient chaos
are active areas of investigation in physical systems,
One way to track the qualitative changes in with strong implications for physiological systems.
the dynamics of a system is the bifurcation dia- Chaotic crises occur where a small change in
gram. The original use of this diagram was to plot some parameter produces a large change in attractor
changes in the solution to a differential equation structure.24,h5
as a parameter is varied. However, it can also be The current diagnostic tools for deterministic
used to plot experimental data, and can reveal tran- chaos require that the process studied is stationary.
sitions to different dynamic states. Figure 3 shows Typically, in a physical system the first 100 or
a bifurcation diagam for a physical system simu- so periods are eliminated from the analysis, and
lation. A horizontal line in this figure corresponds thousands of periods are used for definitive evidence
to periodic steady-state solution or harmonic of deterministic chaos. In physiological systems, non-
component; at bifurcation points two new periodic stationarity is common. and transient signals are
solutions arise. Following some of these bifurcations, likely to be of paramount importance. Fortunately,
a chaotic regime with a broad complex spectrum the new emphasis on characterizing transient dy-
can arise. This sequence of behavioral changes namic states is very timely.‘” Our current limitations
is referred to as the period doubling route to deter- on identifying pure deterministic chaos in the brain
ministic chaos. Byrne has previously provided evi- from physical measurements has become some-
dence that the RI5 burster can proceed through thing of a distraction. The real issues are identifying
this period doubling route to chaos. However, physi- sequences and transitions among dynamic states or
cists have identified additional routes to chaos in attractor structures in brain systems, identifying what
complex systems: intermittency, in which chaotic controls the transitions between these states and
bursts become progressively longer as a system par- determining the extent to which dynamic system
ameter is varied, and the quasi-periodic route to analysis will permit us to find new candidate codes
 Non-linear dynamics of neural systems 591

Period3 Multiple Windows

Increasing Nonlinearity
/
SaddleNode Bifurcation

Driving Parameter
Fig 3. Evolution of the solutions for equations describing a non-linear system (periodically forced
pendulum) as the driving parameter is increased. The system proceeds through a sequence of state changes,
through period doublings or bifurcations and into chaotic states. At some stages, small changes in the
driving parameter can produce dramatic changes in state. We propose that some neural systems may reside
near points of instability in order to effect rapid transitions in state. This plot was produced by simulations
run by M. Shlesinger. A similar mechanical example is developed in detail in Baker and Gollub.4

and representations for behavioral and perceptional with the same parameter values, but experimental
sequences. It is also apparent that analysis techniques neuroscientists usually have no way of deter-
for identifying non-stationary non-linear dynamic mining if a governing parameter is identical. Wang
systems are needed. and Rinzellw have performed a phase plane
One can categorize neural dynamic phenomena analysis of bistable behavior for a pair of inhibitory
either by the nature of the neural activity and its neurons, and demonstrated two mechanisms. One
sequential changes as represented by measurements mechanism involves the decay rate of synaptic
or states or, alternatively, according to the kinds potentials and the other slowly inactivating currents,
of controlling inputs or system parameters which which produce synchronous or alternating oscil-
regulate transitions between dynamic states. The lations in membrane potential. Bistable neuronal
latter approach is similar in spirit to neuroscience discharge patterns can be controlled by application
experiments in which stimuli or chemicals are pre- of neuromodulators. In vertebrates, bistability of
sented and the effects described. For the phenomena discharge in thalamic neurons and motor neurons
present at the level of single neurons, we can divide can be induced by neuromodulators such as
the inputs which promote transitions into three norepinephrine, serotonin and acetycholine, which
broad classes: graded or smoothly varying, sharp are known to be released by diffusely projecting
pertubations and noise. neurons whose activity level varies with behavioral
state.44.M In invertebrates, neuromodulators induce
4. TRANSITIONS PRODUCED BY GRADED INPUTS bistability in neurons by altering intrinsic neuronal
properties. In ensembles, neuromodulators can
One class of neural state transitions that has trigger motor patterns or co-ordinate multiple motor
been described experimentally and analytically patterns.42.82
for single neurons is bistability. Bistability has Another graded parameter that potentially con-
been demonstrated in both vertebrate and invert- trols neuronal and ensemble dynamic state is the
ebrate neurons, including neurons in thalamus,40,64 average level of activity (discharge rate) in the entire
basal ganglia,lo3 inferior olive,57 cerebellar Purkinje network. (The average rate is likely to be some
cellis and stomatogastric ganglion.42.82 Neuro- combination of extrinsic and recurrent input activity,
physiologists use the term bistable to indicate that the transfer function of the neurons and the
neurons have two nearly stable states. To physicists, “spontaneous” neuron discharge. The latter two can
bistability may mean that a system has two states be regulated by neuromodulators.) Three separate
592 T. M. MCKENNA et al.

model analyses have demonstrated that the electro- care maps provide a significant new tool for the
tonic structure and time constants of cerebral cortical neurophysiologist concerned with the dynamics of
pyramidal neurons,’ basal ganglia neurons”’ and single neurons and ensembles.
Purkinje cells” can be strongly modulated by the
level of “background” synaptic input on the den- 6. NOISE-INDUCED TRANSITIONS
drites. The dynamic consequences of such back-
ground activity have not been explored. Its relevance Noise is also an important cause of phase tran-
for neuron dynamics is all the more likely given that sitions in dynamic systems. Noise in neural systems
some extrinsic inputs are often strongly modulated can arise from many sources, including channel noise,
during behavior. Graded changes in synaptic efficacy multiple types of synaptic noise and noise in the
or weight may also control transitions to different sensory inputs and transduction processes. Recently,
dynamic regions. In simple artificiat neural networks two new theories arising from non-linear dynamic
with as few as three neurons, complex dynamics systems have been advanced on the role of noise. In
have been observed which produce bifurcation plots the first theory, noise facilitates state transitions and
similar to Fig. 3, including bifurcations and chaotic the resulting phenomenon, called stochastic reson-
regimes.” The control parameter in this model ance (SR). In the second theory, noise can stabilize
is synaptic weight. While the neurons in such systems in certain regions of their attractors.
simulations are not realistic, the role of synaptic SR is a special example of the result of combining
weight, which can be modified quickly via long-term periodic and stochastic forcing in a multistable non-
potentiation, in ensemble dynamics remains largely linear system. hh In the 1-D case, an overdamped
unexplored in terms of dynamic system analysis. particle in a double well potential is subject
to random forces from thermal fluctuations, and a
5. PERTURBATION-INDUCED TRANSITIONS
periodic external modulation which is weak and
additive (effectively raising and lowering the potential
Perturbations are very effective in shifting dynamic wells). SR arises because of the interplay between
systems from one regime to another (see, for example, the modulating frequency and the mean switching
Moo@). In the neural context these perturbations rate (Kramers’ rate) between wells. This interaction
can be precisely timed synaptic inputs (e.g. the shift accounts for the coherence between the response and
between attractors in the work of Byrne et u/.,‘~ modulation frequency. There is an optimum noise
volleys or synchronized inputs,’ or even transient intensity that maximizes coherence (resonance), and
sensory inputs”‘). Physicists have devised means for in real physical systems the power spectrum exhibits
controlling magnetoelastic chaotic systems, and a sequence of sharp peaks with decreasing amplitude
selecting out stable periodic motions by moving the at odd or all integer multiples of the modulating
stable point and repeller and attractor axes by track- frequency. SR has been examined in electronic
ing the Poincare map, but not necessarily knowing circuits, ring lasers, superconducting quantum inter-
the underlying equations of motion. This technique ference devices, electron paramagnetic resonance.
has been extended to electrical and laser systems, and magnetoelastic beams and in afferent neurons in
successfully applied to control of the heart.” This crayfish mechanoreceptors and monkey auditory
experiment is pa~icularly instructive in indicating nerve.“‘~~4~*x 60.66.67In the electronic systems, the goal is
the potential of dynamic systems techniques in char- to use SR to detect very weak periodic signals in noise
acterizing the dynamics of neural systems. A cardiac by using the noise-enhanced switching between sys-
arrhythmia was induced in an isolated heart by tem states. SR can account for the exact form of the
pharmacological means. At successive stages during multimodal interspike interval histograms of monkey
arrhythmias, the spontaneous period beating passed auditory nerve with tone driving. The data can bc
through period 2 and higher order periodicities into matched by adjusting a single parameter in elec-
an aperiodic regime. A Poincare plot of successive tronic simulations (either noise intensity or stimulus
interbeat intervals was computed in real time. Based intensity).“” *” Hence this very simple physical
on the theory of Ott et al., stable (attractor) and mechanism is sufficient to account for the neural
unstable (repeller) manifolds (axes) (Fig. 4) were data.
computed. By following the successive points on More recently, Moss and co-workers have tested
this return map, these investigators could compute the SR mechanism in crayfish me~hanoreceptors.‘~
precisely when to deliver an electrical perturbation Sharp peaks in the power spectral density of the
or impulse that would bring the next point on the compound action potentials were observed at mul-
Poincare plot close to a stable manifold or axis. tiples of the driving input riding on Lorentzian
When this control was applied. the chaotic aperiodic noise, as predicted by the theory (Fig. 5). Addition-
beating was replaced by periodic beating. The precise ally, the interspike intervals also exhibit peaks
timing of the perturbations required to move the at integer multiples of the mechanical driving fre-
system to a new regime could be computed by quency, and the Poincare plots of return times
tracking the empirical system dymunics in a Poincare show a non-random structure. Many neurons in
section of the phase diagram. Such empirical Poin- the CNS also receive both stochastic and weak
 Non-linear dynamics of neural systems 593

Time (5)

‘1
1

D ’ cl Control
On

I I I

800 1000 1200

n

Fig. 4. Control of heart beat by analysis of chaotic behavior in real-time phase plane analysis. Top right:
recordings of monophasic action potentials during arrythmia induced by ouabain-epinephrine in typical
rabbit septa. Left: Poincare map of interbeat intervals. The parabolic pattern of the intervals is diagnostic
of chaos for an appropriate parameter range. By tracking the sequence of data points in real time, a stable
and unstable manifold can be identified. When interval points occur near the stable manifold, the next
interval point will occur closer to the fixed or stable point. By contrast, in cases where interval points occur
close to the unstable manifold, the next point will occur farther from the fixed point. Tracking the actual
interspike intervals on this Poincare plot permits one to specify the instant at which an electrical stimulus
should be delivered to move the next interval closer to the stable manifold. Bottom right: when this control
technique was applied at every third beat, and maintained on an arrhythmic heart beating chaotically,
period 3 beating was observed, which reverted to chaotic beating when the control was removed. After
Garfinkel er a/.r’

periodic inputs (e.g. 10 Hz in cerebellum and cerebral
cortex and 25-50 Hz in cerebra1 cortex; see sections
on ensemble dynamics).
A new type of phenomenon was recently described
in non-linear electronic circuits which is also referred
to as SR. In classical SR, there are two potential wells
or point attractors; in this new form the “particles”
jump between two chaotic attractors which are gener-
ated by a non-linear electronic circuit developed by
Chua called the double scroll circuit.’ For both kinds
of SR, there is now strong interest in using arrays
of stochastic resonators for tasks such as adaptive
image processing or designing more effective auditory
prostheses. This new type of SR in Chua’s circuit has
not been examined explicitly as a neural model, but
it may be formally equivalent to a simplified version
of Freeman’s model of the olfactory system.”
Noise can also stabilize dynamic systems. In recent
neuron simulations based on Van der Pol equations
for a highly non-linear relaxation oscillator, increas-
ing the noise level added many loops to the attractor
orbits, and increased the density of long dwell times
594 T. M. MCKENNA rt ul.

,060 .080 . 100 .120 ,160 .i60 .200

xE 0
Frequency (kHz)

Fig. 5. Experimental evidence for a stochastic resonance mechanism in crayfish mechanoreceptors.

Bottom: a power spectrum obtained from the compound action potential from crayfish mechanoreceptor
afferents with the associated hair stimulated at 35 Hz. Note the delta-function-like signal at the stimulus
frequency and second harmonic, and the Lorentzian-like noise background. Top left: interspike interval
histogram of mechanoreceptor afferents, exhibiting multi-peaked interspike intervals with amplitude
distribution predictable from stochastic resonance theory. Top right: signal-to-noise ratio (SNR) of
afferent discharge as a function of temperature. The non-monotonic function is predicted by stochastic
resonance theory when temperature is equated with internal noise of the mechanoreceptor transduction
process. After Moss. unpublished; Bulsara cr (11.”

in a saddle-sink region of the attractor.“’ In neural 8. INTERMITTENT SYNCHRONIZED OSCILLATIONS

terms this was interpreted as increasing the influence
of slower membrane events such as adaptation, An intriguing example of non-linear ensemble
and long duration afterhyperpolarization that would dynamics is provided by the intermittent synchro-
promote burst modes of firing. When applied to nized oscillations observed in cortical ensembles.
cortical EEGs, the interpretation given was that These oscillations may appear over a narrow range of
increasing noise amplitude input by non-specific the spectrum (25550 Hz), are synchronous between
brainstem inputs would serve to select and stabilize separate brain sites, last for a few hundred milli-
the EEG in the single spectral mode (one dominant seconds or less, and correlated oscillations are
peak in the EEG spectrum), multiple mode and then observed at multiple sites in sensory regions in
spindle-burst patterns. response to particular sensory configurations’4.26”
or between sites in sensory and motor regions at
particular phases of a sensorimotor task.y.71.79Cross-
7. NEURAL ENSEMBLE DYNAMICS AT THE MESOSCALE correlogams for neural activity recorded from two
separate electrodes show peaks at phase lags between
Evidence of non-linear dynamics is also emerging 0 and a few milliseconds. This phenomenon and other
at the level of neural ensembles. We review some examples of “anomalous dispersion” (Ref. 29 and
examples in this section. Unfortunately, there has not see below) appear to have too short a time lag to be
yet emerged a systematic account which relates the accounted for by direct axonal conduction velocity,
single neuron dynamics to the ensemble dynamics, reflecting either common driving or non-linear system
nor uniquely characterizes the dynamics of these properties.
levels, nor identifies the specific neural substrates In the case of cat visual cortex areas 17, 18 and 19,
which dominate the dynamics at different levels. these synchronized oscillations or neuronal bursts
An important exception is provided by Freeman’s” can be recorded at nearby sites or at sites separated
earlier work, which analysed the olfactory bulb from by 7 mm.” Cross-correlograms reveal synchronized
cellular to ensemble levels using classical systems 25-50 Hz oscillations during activity driven by effec-
theory. tive visual stimuli in the respective receptive fields
 Non-linear dynamics of neural systems 595

(RFs) of the two sites. The degree of synchrony bats, described below, show a systematic relation
depends on the stimulus configuration, e.g. single between phase shifting of oscillations and stimulus
bars across both RFs produce stronger cross-corre- parameters.23,39
lation peaks than do separate bars in the same The biosonar of the bat enables it to discriminate
direction crossing the RFs, while two bars in opposed fine surface features of targets as well as minute
directions to the RFs give zero cross-correlation. differences in the distance of different target surfaces.
Although these oscillations are elicited by the In psychophysical tasks, bats are capable of echo
visual stimulus, they are not locked to the stimulus. resolution in the 1 ps range.87 This raises a problem
Cluster recordings from multiple neurons, and some- for auditory neurophysiology. How can single neur-
times single neurons, exhibit the rhythmic bursting. ons which operate in the millisecond range reliably
Neurons at a given site can shift from one syn- encode microsecond differences in acoustic signals?
chronous ensemble to another depending on the Simmons’ data suggest that the solution is found at
stimulus conditions.25 For example, for four cortical the neural ensemble level, and involves the systematic
sites with overlapping RFs, cells can be synchronized phase shift of population oscillations in response to
in all possible pair combinations in response to acoustic stimuIi.23,39 Multi-unit recordings in inferior
single light bars with the appropriate orientation, but colliculus of the big brown bat revealed that oscil-
simultaneous presentation of two different orien- lations are evoked in response to FM sweep pairs
tations can selectively synchronize a small subset corresponding to emission and echoes, presented
of pairs of sites depending on their orientations. binaurally via earphones. As seen in Fig. 7, the
Transient synchronized oscillations are also observed average population waves last four to seven cycles, at
in non-anesthetized monkey visual area MT49 and approx. 20 Hz. As the interaural delay is systemati-
anesthetized area Vl in squirrel monkey.50 cally varied over a range of O-SO ps, the oscillatory
Transient coherent activity has also been observed responses to the emission-echo pair are phase ad-
between visual and sensorimotor cortical sites in vanced by several milliseconds. The phase-shifted
behaving monkeys, although the spectral content is oscillations produce a time expansion of the echo
much broader than reported for cat sensory cortex. delay by a factor of 20-50. Moreover, the cycle
Bressler and Nakamura9 recorded evoked potentials by cycle structure of the local averaged response (at
at multiple sites in visual, parietal and sensorimotor best frequency sites) may be a model of the echo
cortex in monkeys performing a go/no-go discrimi- waveform; a 360” echo shift produces a 360” response
nation task. During the response in the go condition, phase shift. Similar oscillations have also been
a subset of paired sites in visual and sensorimotor observed in bat auditory cortex (Simmons, unpub-
cortex showed a strong peak in coherence (cross- lished observations). Phase plane analysis of the
power). The coherence peak. was spectrally broad cortical oscillations reveal that the waves are non-pe-
over the range of O-100 Hz, with amplitude falling off riodic and have a deterministic structure (Solinsky
in a l/fmanner. However, with band-pass filtering in and Simmons, unpublished observations). Further
the gamma region, oscillations are evident in individ- analysis of the waves and the possible non-linear
ual records from visual and motor cortex, which are oscillators that could generate such waves are under
in phase for four to five cycles just preceding the peak way. Although the mechanism by which an interaural
of coherence in the unfiltered records (Fig. 6).9 delay results in a particular phase shift of the inferior
Murthy and Fetz” observed synchronous 25-35 Hz colliculus oscillation is unknown, these results indi-
oscillations and zero phase lag in sites 20 mm distant cate that phase differences in ensemble oscillatory
in somatosensory and motor cortex of behaving activity are capable of encoding stimulus dimensions.
monkeys. The transient nature of the synchronous Simmons has further interpreted the results to indi-
activity in sensorimotor areas is further evident in cate that multiple time scales can be encoded in the
the observations of Sanes and Donoghue.79 Local neural population oscillation responses (i.e. millisec-
field potentials were recorded simultaneously at up ond scale for emission-echo delay, microsecond scale
to 12 sites in the motor and premotor cortex of for interaural delay and echo waveform).
monkeys performing visually guided, instructed delay Llinas and associates55~78 have observed in human
tasks using wrist or finger movements. Oscillations magnetoencephalogram (MEG) recordings a 40 Hz
at 25-50 Hz were observed most frequently prior oscillation which sweeps from rostra1 to caudal
to the signal to start movements. Significantly, the in cerebral hemispheres. Acoustic stimuli reset this
synchronization was observed at long distances oscillator, and a synchronized, higher amplitude
and at individual sites the periodic waves could be 40 Hz oscillation is produced for 100-200 ms follow-
synchronized for many cycles, phase-shifted or go ing stimulus onset. This synchronous activity is
in-and-out of phase within a few cycles. Neither phase-shifted rostra1 to caudal, so that a phase shift
the relevant sensory, motor nor behavioral variables, of 46 ms is seen from frontal to occipital-temporal
and the full topography of these phase differ- cortex. These results indicate that the use of resettable
ences between neural ensembles, have been charac- and synchronizable oscillators may be a broadly used
terized in these experiments. However, striking neural phenomenon. Llinas et al. have also obtained
new results from Simmons on auditory system in direct evidence for thalamocortical involvement in
596 T. M. MCKENNA et al.

Unfiltered

Normalized
amplitude

Correlation’

Time (ms)

y-Filtered
.-
Normalized
amplitude

f Striate

Correlation*

.5

Time (ms)

Fig. 6. Time series of coherence (normalized cross-power) between electrode sites in motor and striate
cortex in monkeys performing a go/no-go task. (A) Unfiltered waveforms of striate and motor cortex for
a single go trial, with squared cross-correlation plotted below. (B) The same waveform with digital
band-pass filtering in the gamma-frequency range (3 dB down at 30 and 80 Hz). After Bressler and
Nakamura;’ Bressler, Coppola and Nakamura, unpublished.

the 40 Hz oscillations. Layer 4 neurons in neocortex of neural assemblies which propagate synchronous
exhibit subthresho~d oscillations in this range” and activity along diverging and converging pathways,’
thalamic projection neurons can produce rebound and the theory that temporal synchrony could
oscillations at 40Hz.‘06 They have pointed out that underlie visual segmentation and that correlated
thalamocortical resonance could be a factor in the activity within a group of cells can reflect their
widespead synchronizations. dynamic grouping. 9y In fact, the original observation
Previous interpretations of the synchronous oscil- of synchronous oscillations in visual cortex by
lations (eg. Koch45) have emphasized a distinction Gray et a1.35 led Crick and Koch2’ to hypothesize
between the synchronous nature of the activity and that this activity constituted a neural substrate of
the oscillations, which may or may not be evident sensory binding, in this case binding elements of a
in individual records. Evidence for synchronous sensory stimulus into a coherent entity. Recently,
activity between neural ensembles has been more Lhnas and Pares4 have hypothesized that the tem-
readily accepted than for oscillatory activity, perhaps poral correlation between sensory inputs and wide-
in part because prior theoretical analyses of cortical spread endogenous thalamocortica1 rhythmic activity
activity have emphasized the significance of coinci- (40 Hz) is an essential component of the perception of
dent inputs. Examples of this are the “synfire” chains that sensory input.
 Non-linear dynamics of neural systems

12.5
lime (ms)
Fig. 7. Neural ensemble oscillating responses in bat inferior colliculus with phase shift dependent on
interaural delay. Top left: spectrogram of emitted call of bat Eptesicus. Top right: diagram of stimulus
delivery system. The bat’s sonar emissions were picked at microphones (m), digitally delayed and then
returned to the bat from loudspeakers (s) as echoes. Bottom: responses to emission and echo (6 ms between
emission and echo) recorded from small groups of neurons in the inferior colliculus with glass
micropipettes with impedance of 5-10 Ma. Each trace represents an average response (n = x) to the
emission-echo stimulus, at a particular interaural difference in presentation of the echo, with the delay
indicated in microseconds. Note the systematic phase shift, in milliseconds, as the interaural delay is
increased, in microseconds. After Haresign ef af.‘9

The notion that synchronous activation can be
used as a substrate for cognitive binding has been
exploited by Shastris3 in his novel approach to hybrid
neural architectures. Shastri and Ajjanagadde@ have
developed a spatiotemporal neural net in which the
strength of activation and firing time of a node
depend explicitly on a spatiotemporal integration of
input signals, and the representational state of the net
depends on the relative firing times of nodes. They
have used this connectionist net to encode complex
conjunctive rules and perform inferences. The model
achieves these by representing dynamic bindings
as the synchronous firing of appropriate nodes,
and representing rules as interconnection patterns
which direct the propagation of rhythmic activity.84
Naturally, this system goes well beyond current
neuroscience and the nodes are not realistic neurons,
but it is indicative of how much computational
potential resides in the simple notion of synchronous
neural activity.
The neural ensemble oscillations, per se, have
been somewhat sceptically received, perhaps in part
because reductionist neurophysiologists are more
comfortable with bursting in individual neurons than
with waves in neural ensembles, particularly in the
sensory domain. It may also result from the influence
of linear sytems-based engineering, in which instabil-
ities are designed out of systems, but device physics
lead to imperfectly implemented designs. In fact,
it has been suggested that the oscillations are
“epiphenomena”.~ Additionally, there are currently
conflictirig experimental results.34.‘07 Indeed, aperi-
odic activity with a broad spectrum is a common
observation in many, if not most, neural regions.
For those who wish to characterize the non-linear
dynamics of neural activity, this observation is more
challenging than periodic oscillations, but also more
interesting.
Moreover, from the dynamic systems view, we
wish to draw attention to the significance of the
598 T. M. MCKENNA PI al.

intermittent nature of the activity, the possible sory input can drive the olfactory cortex from a basal
physiological control of the phase shift and the nature attractor observed during spontaneous activity into
of the waveform of the periodic waves, when they attractor wings that correspond to the learned signal
are present. class.“,*04
Intermittency is characteristic of dynamic systems
near instability and could indicate the transition from
9. SPATIOTEMPORAL MODES OF ACTIVITY IN
one attractor regime to another. The control of the THE BRAIN
phase shift, as indicated in Simmons’ experiments,
needs to be explored in terms of biophysical mechan- New tools for dynamic imaging of brain
isms and the analysis extended to other sensory and activity, such as voltage-sensitive dyes and coherence
sensorimotor systems. As we will see later in analysis of MEG or EEG recording arrays, have
the section on motor controt by coupled non-linear been used to explore the spatiotemporal domains of
oscitlators, phase shifting between coupled non-linear activity correlated with ~havioral states and sensori-
oscillators may be a key factor in producing co- motor processing. The spatiotemporal pattern of
ordinated movement. Finally, the nature of the wave- activity in brain is a fertile area for dynamic system
form will help to identify the dynamic state of the analysis.“’
generator and how it could serve as a signal to In one recent series of experiments, Kelso and co-
another ensemble. Of relevance to the latter issue is workers analysed a phase transition in both human
the recent work on synchronization of chaotic behavior and neuromagnetic field patterns.“,4” MEG
systems, an achievement previously thought imposs- recordings were made with an array of 37 supercon-
ible given the sensitivity to initial conditions of ducting quantum interference devices in human
chaotic systems. Recently, two physicists, Pecora and subjects performing a task in which they were in-
Carro1,‘8.74.75designed a system for synchronizing two structed to syncopate a manual response between
chaotic systems within a few milliseconds by sending tones delivered at one per second and higher rates.
a control signal from one system to another. A parent As the rate of tone presentation rose, a stage was
chaotic system generates a complex signal which reached ~‘transition”) where subjects suddenly lost
causes synchronization with duplicate subsystems. syncopation and shifted to a predictive mode, where
The criterion for this synchronization is that the sign the response became synchronous with the next
of the Lyapunov exponents of the subsystems is tone, This is evident at a jump in response latency,
negative, which means the subsystems are stable measured in terms of relative phase of the tone
in the absence of a driving signal. This scheme has delivery cycle. This transition in sensorimotor behav-
been demonstrated in electronic circuits. This type ior is accompanied by a change in the power spec-
of synchronization is important when one cannot trum of the MEG and in the spatial pattern of
use periodic forcing of timing signals because the activity. Spatial analysis of the coherence (cross-
responding subsystem is operating in the multiperiod power) revealed that, at the behavioral transition,
domain (e.g. period doubling). Neural ensemble ac- the spatial locus of maximum cross-power expands
tivity generally exhibits multiple spectral peaks: considerably, then shrinks back to the pretransition
moreover, the modular or~nization of neural locus at higher presentation rates (see also the discus-
architectures (identical subsystems?} is ubiquito~ls. sion of transient correlation structures in cerebellar
Extending the analogy further, one can imagine cortex in a later section). The recorded activity also
master signal generators which may be aggregates showed a change in phase of the response and
of modules or subsystems which have acquired an topographic distribution of phase relation to tone
additional degree of freedom, generating pseudo- stimulus when the transition point was reached.
periodic signals to co-ordinate additional modules in Eigenfunction decomposition of the spatial pattern of
a motor or sensory sequence. Alternatively, special- MEG activity reveals a large drop in the most
ized global systems, such as non-specific systems,54,b’ dominant mode at the transition. They are currently
may serve this role by driving the subsystems using this spatial mode information to infer the
into regimes where they co-ordinate their activity in dynamics of the neuromagnetic field generators.
qualitatively different manners. in terms of coupled non-linear oscillators. Kelso
The technique of Pecora and Carrel is related to concludes that the results support his view of the
Haken’s’” concept of synchronization of systems near brain as a self-or~njzjng pattern-forming system that
singuiarities like bifur~tjons. The point is that if two operates close to instability points, which allows it to
neural ensembles are near critical points in their switch llexibly and spontaneously from one coherent
dynamics, an appropriate periodic or more complex state to another.
signal with the correct waveform can synchronize The development of voltage-sensitive dye recording
their activities within a few cycles. The results arc has produced significant mappings of the spatial
analogous to those of Freeman in his olfactory organization of the visual cortex. Static features such
model; when a sensory cue has been learned. as orientation domains, ocular dominance bands.
the particular spatiotemporal pattern of oscillations etc., have been revealed in great detail8 Recently, this
resulting from the non-linear processing of the sen- technique has been extended to dynamic mapping of
 Non-linear dynamics of neural systems 599

brain activity. 85,9oIn response to moving bar stimuli, context and history-dependent manner.29.30,9’ The
Kaplan and colleagues recorded the entire spatio- phase patterns can also be regarded as a case of
temporal pattern of neural ensemble activity within a anomalous dispersion. The evidence for this is based
3 mm x 3 mm window of visual cortex using voltage- on the observations that the speed of the phase
sensitive dyes. The complex sequence of spatio- gradient of the coherent oscillations is much greater
temporal patterns observed were analysed by a than either calculations of synaptic and axon delays
“snapshot” technique of Karhunen-Loeve decompo- or the speed of the spread of evoked potentials
sition, which has also been used recently for the elicited by focal electrical stimulation of the bulb.
analysis of patterns of turbulence. The spatial eigen- Because the olfactory bulb has a repeating micro-
functions capture the salient features of the pattern circuitry, Freeman has produced a model based on
of activity. By averaging over the spatial array, the interconnected modules which are composed of
time course and power spectrum of the individual lumped parameter models which represent distinct
eigenfunctions were computed. Peaks at 9, 21 and neuron types. Due to realistic feedback loops within
36 Hz were evident in the first eigenfunction from the olfactory bulb, anterior olfactory nucleus and
cat visual cortex. This preliminary study has shown prepyriform cortex, each are capable of oscillation
that it is technically feasible to analyse the tremen- with a different characteristic frequency. The bulb
dous amount of multidimensional data generated by oscillator output can exhibit a positive Lyapunov
voltage-sensitive dyes for dynamic stimuli. Among exponent, and the distributed delay lines and positive
the many questions that remain to be addressed and negative feedback connecting these three brain
are the relationship between the eigenfunctions and areas lead to a large dynamic repertoire, including
known cortical structures, such as ocular domin- aperiodic chaotic waveforms. The entire system can
ance columns, orientation columns and color blobs. simulate the real EEG. The basal attractor appears in
Another issue is the relationship between the stimulus phase space as a collapsed hypertorus. A dynamic
parameters and the eigenfunctions. More impor- non-linearity within the bulb, which arises because
tantly, can a model be synthesized to account for the gain depends on the input amplitude, produces a
the spatiotemporal pattern, and can a new dynamic spectrally rich burst of activity on each inhalation.
theory emerge from this analysis. One of the issues In the animal experiments, discriminant analysis of
raised in an earlier section, the topography of syn- the spatial configuration of the amplitude modulaton
chronization, might also be addressed by performing of the 64-electrode array permitted correct classifi-
local averages of the eigenfunctions to observe local cation of learned odors. Based on these results,
time series of eigenfunctions or cross-power analysis a version of the model was implemented with 64
to search for coherence patterns. The use of eigen- modules within the olfactory bulb (KIII model’“).
function decompositions is part of a larger search for This model was tested on a difficult classification
the natural basic functions of spatiotemporal brain task involving the identification of industrial parts
activity. In the case of turbulent channel flow, the use from the pattern of ultrasound scatter. The scattered
of empirical eigenfunctions led to the discovery ultrasound was collected at eight sensors, and
of hitherto unknown phenomena (propagating turbu- these signals provided 64 vector inputs to the
lent wavesssm90), and the eigenfunctions themselves KIII model. The model outperformed a statistical
can be used in specifying mathematical models that classifier, backpropagation neural networks and
produce the main features of the attractors under- Hopfield network in classification accuracy.lo5 It was
lying the physical system. Hence, this approach observed that when the network learned a new signal
appears very promising for analysis of patterns of class, a unique set of attractors was observed in
neural activity revealed by voltage-sensitive dyes, and the phase plots of co-varying activity in the different
the synthesis of dynamic models of the cortex. neuron types.‘“,io5 This raises the issue of the con-
Perhaps the most extensively investigated and ditions under which neural system or module attrac-
modeled neural system with regard to spatiotemporal tors can represent signal class. Based on experimental
patterns of activity is the olfactory system.29.30,63Sim- results, in the simulations, learning produces Hebbian
ultaneous recordings from as many as 64 sites in the synaptic strength changes in the excitatory feed-
olfactory bulb reveal a complex spatial pattern of back connections. These synaptic changes produce a
oscillations riding on the respiratory rhythm when a bifurcation in the system. Learning adds a new
rabbit inhales a learned odor. The spatial pattern attractor, with a lower dimension, to the attractor of
of the phase of the burst is consistent with a self- the basal state.
organizing, co-operative dynamic rather than an Freeman’s analysis of the olfactory system pro-
external pacemaker. This is based on the observation vides a number of observations which are highly
that the phase pattern in the bulb is a cone in circular relevant to the discussion of the significance of the
co-ordinates, whose apex varies spatially at random sychronized oscillations seen between sites in visual
and whose sign can shift from lead to lag, obser- and sensorimotor cortices. One is that multistage
vations which are inconsistent with pacemaker neural systems may take advantage of the spatio-
activity. The spatial configuration of the amplitude temporal pattern of synchronized activity to extract
modulation of the oscillations encodes odors in a weak signals from noise. For example, the olfactory
600 T. M. MCKENNA et uf.

bulb exhibits spatiaIly distributed synchronized both forward and backward locomotion? The neural
carrier waves in response to specific peripheral events. circuitry underlying motion co-ordination has been
The bulb, in turn, projects to the prepyriform cortex, successfully modeled as a chain of coupled non-linear
where bulb input is widespread and diffuse, and oscillators.4R~‘0’*‘02In the model, each segment has a
where individual neurons receive widely convergent pair of oscillators, each with an intrinsic frequency
input. Because of this divergent-convergent pattern and a limit cycle attractor in phase space. When
of connectivity, the spatially coherent oscillations of coupled to its neighboring oscillators (rostrocaudal),
the bulb become reflected in the neural activity of the each oscillator will increase or decrease the frequency
cortex with broad spatial distribution, even though of the receiving oscillator in proportion to the
the input coherent signals are embedded in large phase difference between the sending and receiving
uncorrelated noise activity. Second, the form of the oscillators. A simple set of linear ascending and
oscillations is significant. The information resides in descending coupling functions (frequency change as
the spatial distribution of the amplitude moduIation a function of intersegmental phase lag) can be
of the carrier. Third, the target regions, by virtue defined which produces stable backward or forward
of their own dynamics, temporal dispersion, feed- swimming. This simple system satisfies the constraint
back connections and possible plasticity of intrinsic that phase lag between segments is independent of
connections, particpate in and modify the global speed. In the lamprey the specific neuron types and
dynamics of the system. 3oFourth, this type of analysis connectivities of these segmental oscillators have been
points out how a hierarchy of neural levels might take characterized. This general model can be mapped
advantage of non-linear dynamics. Neural ensembles into a model with specific neural circuits.” These
capable of chaotic behavior are sensitive to initial simulations also satisfy the locomotion constraints
conditions; hence, in principle, small patterns of and the critical connections can be identified. Unfor-
activity in a few neurons could induce a global tunately, for many motor systems, we lack this
pattern shift in the ensemble. cellular detail, but dynamic models can provide
significant insights into essential properties which can
focus the search for neural substrates. There are
10. COUPLED NON-LINEAR OSCILLATORS fN MOTOR
CONTROL: CHAINS OF OSCILLATORS a number of advantages in the use of coupled non-
linear oscillators for motor control and robotics.
In earlier sections, we described observations Where the individual oscillators generate limit cycles,
of synchronous oscillations in sensory and motor they are stable in the face of perturbations. Addition-
systems. While there have been some attempts to ally, in this model, the coupling of the oscillators
produce models which can account for the zero small confers additional adaptiveness in response to pertur-
phase lag in these oscillations,‘5~4’.45 47 these models bations or drift: an increase in the phase difference
have not predicted the generation of spatiotemporal produces an increase in coupling, with an attendant
patterns that could specify sensory or motor behav- increase in ensemble frequency and hence a decrease
ior. There have also been preliminary attempts to in phase differences between segments. (Williams has
identify the generator of spatiotemporal patterns of suggested that this mechanism may also apply to
neural activity in terms of coupled oscillators? Aside synchronized cortical oscillations.)‘“’ This approach
from the work of Freeman, these analyses have not simplifies the motor control problem. lnstead
proceeded very far. of tracking movement trajectories, which may be
However, in the case of neuronal generation of difficult to adaptively compute in real time for limbs
motor control, there has been success in accounting and may be unreliable in the face of outside forces,
for the adaptive rhythmic generation of activity the system tracks and adjusts limit cycles of the
for locomotion.5~‘~~36~7”~*6~‘o* During swimming in the oscillators which control components of the move-
lamprey, a traveling lateral mechanical wave propa- ment. This produces a rapid adaptation lo internal
gates down the body, producing forward propulsion. and external perturbations and drifts. This approach
Recordings from spinal ventral roots or segmental also implies a broader strategy for motor control, in
muscles show a rhythmic output at each segment (the which neural systems embody a library of non-linear
lamprey has up to 100 segments).‘” While the time oscillators that can be coupled in different ways to
lag between activity bursts in different segments is a enable flexible, real-time movement control. We will
function of swimnling speed or cycle duration, the explore this idea again in relation to the cerebellum
phase lag per segment is a constant proportion of with its 2-D sheet of neural elements.
the cycle period, independent of speed. This leads to Paired chains of oscillators have also formed the
approximately one wavelength of this traveling wave basis of models of legged locomotion. Following
being on the body at all times, and this minimizes the suggestion of Pearson, models of six coupled
lateral forces. Hence, the constant proportion phase oscillators can produce sequences of gaits in hexa-
lag is a significant constraint on co-ordinated loco- pods that confer stability during locomotion at differ-
motion in the lamprey. How can neural circuitry ent speeds.’ These models have been recast in
produce co-ordinated motor output that fullils this terms of dynamic systems.h.h2 The advantages of this
constraint over a range of swimming speeds. for formulation are terms of analysis, particularly in the
 Non-linear dynamics of neural systems
absence of complete knowledge of the specific neural
circuits, and in the ability to explicitly regard the
organism and the physical environments as a coupled
dynamic system.6 System dynamics are also essential
in the biomechanics of legged locomotion, as evident
in the analysis of dynamic stability of cockroach
running.” Under conditions of static stability (slow
locomotion), the center of gravity is maintained
within a tripod of legs in contact with the substrate.
However, during rapid running, the tripod gait is
replaced by an “effective leg” (sum of leg force
vectors), with a trajectory which orbits the center of
gravity during the stepping cycle.96
11. MAMMALIAN OLIVOCEREBELLAR SYSTEM AS A
TWO-DIMENSIONAL ISOCHRONOUS SHEET OF
COUPLED OSCILLATORS
The cerebellar lobules contain detailed but complex
maps of the body via tactile and proprioceptive
inputs, receive relayed input from the other motor
regions such as motor cortex and map systematically
onto motor output (premotor) systems. The cerebel-
lar cortex has a very regular cellular architecture,
which includes a monolayer of large Purkinje neur-
ons, each receiving about 100,000 synapses from a
beam of parallel fibers and one large climbing fiber
originating in the inferior olive (IO), which synapses
repeatedly on the Purkinje cell dendrites. The IO also
receives somatosensory input and contains neurons
which are locally connected by gap junctions.
By virtue of intrinsic neuronal properties and the
coupling it generates a 5-15 Hz rhythm.52 The coup-
A. NON-MOVEMENT PERIODS
@@ . .
. . . .
. .
Fig. 8. Cross-correlation patterns among simultaneously
Top: magnitude of cross-correlation coefficient of discharge of Purkinje neurons relative to neuron at
site M, for non-movement periods (A) and movement periods (B). Note ephemeral correlation
during movement. Bottom: topography
601
ling of these neurons is controlled by feedback from
the Purkinje neurons via the deep cerebellar nuclei
(including dentate nucleus). The inhibitory synapses
of the deep cerebellar nuclei (e.g. dentate nucleus)
synapse directly on the gap junctions between the
IO neurons.92 Hence, cerebellar input is capable of
fractionating the IO oscillator into local domains.
The conduction velocity of the IO axons to cerebellar
cortex is biologically regulated so that the time of
arrival of all IO fibers to the cerebellar sheet is
identical, i.e. the cerebellar cortex is an isochronous
sheet in terms of olivocerebellar transactions.93 Llinas
and co-workersS’,80*8’have recorded simultaneously
from 30 to 96 single Purkinje neurons in the cerebel-
lum of the rat. Cross-correlation analysis of record-
ings reveal that rostral-caudal beams of Purkinje
neurons are correlated with a 10 Hz rhythm which
depends on IO input, and whose pattern is consistent
with the anatomy of IO-cerebellar projections.
Under the same conditions, activity of neurons in the
mediolateral dimension of the Purkinje cell array is
not correlated. This basic pattern requires the active
involvement of the cerebellar inhibitory feedback to
IO via dentate.5’ By contrast, preceding and during
movements, a complex pattern of mediolateral corre-
lations is seen transiently over long distances in
the cerebellar array (Ref. 80; Llinas, unpublished
observations) (Fig. 8).
This leads to a new view of the coding of
movements in cerebellum. In this view, the 10 Hz
oscillation and motor tremor generated by the olivo-
cerebellar system play a role in co-ordinating move-
ments by providing a clock for synchronization.”
8. MOVEMENT PERIODS
0.03
0
0.M l
&ml .
recorded Purkinje cells in rat cerebellum.
pattern
of electrode array in rat cerebellum. After Llina$’ Llinas,
unpublished.
602 T. M. M~KENNA et al

Moreover, it is hypothesized that these transient activity at different levels of the nervous system. The
correlation structures in the Purkinje cell array are familes of attractors in phase space that characterize
coding the movement. A large number of motor complex non-linear physical systems can prove
programs can be stored by means of the large valuable in describing a range of behaviors and
number of correlation structures possible in the associated neural activity, including sensory and
large 2-D Purkinje cell array. Compared to the motor repertoires, in neural systems. These tech-
chain of oscillators described in the lamprey signal niques can identify functionally significant states of
cord and invertebrate ganglia, the olivocerebellar single neurons and neural ensembles not apparent by
system provides much greater flexibility and capacity more traditional methods of analysis. Transitions
for movement programs. In a chain of oscillators between attractors and transit times within attractors
local connectivity among local oscillators domi- may serve as useful descriptors for analysing state
nates and the repertoire is limited. In the 2-D changes in neurons and neural ensembles, including
Purkinje cell array, a large number of combinations state changes induced by sensory inputs. Among the
of Purkinje neurons can be linked in a correlation likely neural parameters that regulate dynamic state
structure by the IO-cerebellar loops. Hence, the transitions are neuromodulators, synaptic weights
mammalian motor system has placed the oscillators and the non-specific systems that determine back-
in a separate neural structure which can be frac- ground level of neural activity in ensembles. Pertur-
tionated into local oscillators under control of the bation-induced state transitions may be produced by
cerebellum. This strategy may lead to greater flexi- precise timing of synaptic inputs or synchronous
bility while retaining the speed advantages of motor inputs relative to the phase of endogenous cycles of
control by coupled oscillators. Obviously, further activity. Noise-induced transitions may enhance the
work is needed to specify the relation of the corre- responses to weak periodic inputs of neurons via
lation structures to movements, but this approach simple non-linear physical mechanisms.
could potentially provide exciting new insights into The recent observations of synchronous cortical
the dynamic population coding of motor control. oscillations in the 25-50 Hz range may provide
This approach should also be extended to motor insight into neural ensemble dynamics. From the view
cortex in order to specify the unique roles that of non-linear dynamic systems, neural subsystems
these two neuronal arrays play in motor control arc being co-ordinated or synchronized. Key factors
and planning. This new approach requires state-of- from the dynamic systems viewpoint are the phase
the-art recording techniques combined with the shift and its systematic control, the intermittent
appropriate analytical tools for dynamic system nature of the synchronization and the identification
characterization. Fortunately, the repetitive nature of the waveform and its modulation across the spatial
of the cerebellar architecture provides significant dimensions of the neural array. New techniques
experiment advantages. for the visualization of spatiotemporal dynamics
in neural ensembles (including voltage-sensitive dyes,
12. CONCLUSIONS arrays of recording electrodes for single neurons.
MEG and EEG) provide opportunities for observing
In summary, the brain can be regarded as a coherent spatial structures, and the natural basis
dynamic system that is non-linear at multiple levels functions of neural population activity involved
of analysis. A characterization of its non-linear in the control of movement and perception. New
dynamics is fundamental to our understanding of developments in the experimental physics of complex
brain operation. An extensive array of recently devel- systems, such as the control of chaotic systems,
oped mathematical tools for analysing non-linear selection of attractors, attractor switching and transi-
systems in physics can be used to great advantage by ent states, can be a source of powerful new analyt-
the neuroscience community. For example, phase ical tools and insights into the dynamics of neural
space analysis can be applied to describe neural systems.

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(Accepted 25 October 1993)