Matched filtering—a possible function of the basal ganglia?V. T. Shuvaev

I. P. Pavlov Institute of Physiology, Russian Academy of Sciences, St. Petersburg~Submitted February 24, 1999!Opticheski� Zhurnal66, 41–45~October 1999!

This paper discusses a number of the soundest viewpoints on the function of the basal gangliaand data obtained by the author and his coworkers from a study of the structure of thepulse activity of the prefrontal cortex, the neostriatum, and the amygdala in dogs and the lowerprimates, the influence of electrical stimulation and pharmacological effects on thecholinergic system of the caudate nucleus on the implementation of the motor behavior of dogs.On the basis of a comparison of the data, it can be assumed that a possible function of thebasal ganglia is to fine-tune implemented behavior according to the principle of matched filtering.© 1999 The Optical Society of America.@S1070-9762~99!00710-1#

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A number of concepts have appeared that subdivideforebrain into at least three large sections: the neocortexstrio-pallidal system, and the limbic system.12,13 Each ofthese sections possesses its own range of functions inorganization of behavior. It is acknowledged by many scitists that the most puzzling functional role seems to be thathe basal ganglia~BG!, which possess an extremely complmorphological and neurochemical organization.

B. F. Tolkunov, in his theoretical paper3 on the prin-ciples of determining the function of the ganglion, arrivedthe conclusion that the function of an organ must be demined from the internal characteristics of the processesoccur in it and not from the actions produced by them.determined the operation of the ganglion as the receptioinformation and its processing into the executive commanecessary at a given instant.

In the multilevel organization of the brain, the BG ocupy a very high-level position, having no linear relatiowith either external action nor with an observed effect. L.Kachalova2 comes to the conclusion that it is impossiblethis case to define the ‘‘function’’ by analogy with sensoand motor systems. She bases her conclusion on the foling facts:

• The caudate nuclei~CN! has no direct influence on thmotor neurons.

• The main cortical and thalamic afferent cells are cocentrated in these nuclei, but they include no projectionsthe trunk relays of the visual and auditory analyzers.

• There are few direct paths from the cortical sectionsthe analyzers, and their role in the transmission of sensinformation is doubtful.

• The activity of the neurons of the CN correlates wthe behavioral meaning of the sensory stimulator, andwith its parameters. These neurons are associated withattention process, the state of expectation, and the antiction of the result of activity.

• Signal processing at the level of the CN is differentprinciple from that in sensory systems: The direction alocalization of a stimulus are coded at this site, andanalysis of the information is oriented toward action.

Divak proposed8 that the BG convert cognition into action, and later9 that the BG can be intermediators in the ph

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nomenon of motor equivalence—the ability of an organito achieve goals by means of various motions, a set of anative motor patterns. That is, the BG play a role in ttransition from decision to motion.

On the basis of three classes of facts: the high degrewhich the responses of the neostriatum to peripheral stimare subordinated to corticifugal signals from the zones ofcorresponding sensory representations; the selectivity ofcorticifugal influences on the neostriatum; the capacity olocal signal from an individual cortical sensory represention in various degrees to alter the responses to a gistimulus in all the regions of the neostriatum, both in thowhere a fiber arrives from a given zone of the cortex andthose where the afferent cells arrive from other sections oV. F. Tolkunov3 showed that functionally specialized corticifugal signals in the neostriatum act on it in accordance wits specialization and, being transformed in it, are translainto another metric. The two-dimensional mosaic-discrrepresentation intrinsic to the cortex is transformed intogeneralized matrix form, which reflects the situation in tcortex by its state as a whole. Because of this, the effeoutputs from various sections of the neostriatum introduthe result of the cortical activity into each structure of tbrain innervated by the neostriatum.

The most reasonable assumptions concerning the futional affiliation of the BG in the organization of behavioare expressed by Rolls.15 On the basis of his own data anliterature data, the author showed that the functions areregated in different zones of the corpus striatum. His dshow that apparently not all the information presented incortex arrives at the head of the CN, the tail of the CN, athe posterior putamen. The corpus striatum most likelytains the result of an evaluation carried out by the cortizone projected onto it and can use it for switching or alterbehavior. Rolls’s article sets forth the hypothesis that certparts of the corpus striatum, especially the head of the Cthe ventral striatum, and the posterior putamen, receiveresult of evaluations connected with memory and cognitprocesses but do not carry them out themselves. The costriatum can be involved in the switching of behavior thdepends on conflicting information received from the cortiand limbic regions of the cortex; i.e., the corpus striatu

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participates in the choice of behavioral responses and information of a single flux of behavioral output. At the samtime, there is a possibility of switching it if a high-prioritinput is received from an upper level of the organizationthe brain. Rolls’s paper also expresses the assumptionthe BG are capable of detecting a combination of conjugaactive inputs from zones of the cortex that are rather remfrom each other, using its own network architecture, as was the property of synaptic modification. Consequently,possibility appears of triggering any complex pattern of bhavioral responses~learned by trial and error, with a finadecision that henceforth is associated with the trigger ofinput events! appropriate to any complex situational patteusing an associative neural network.14,16

A consequence of this hypothesis is the assumptionmotor plans are stored in the BG that can be regardedseries of snapshots of the corresponding input pattern inevolving sequence of input information. The corpus striatuthe globus pallidus, and the substantia nigra form a two-lesystem that participates in the selection of behavioralsponses when inputs compete and in the appearanclearned responses corresponding to a specific situation.

The original viewpoint on the participation of the BGthe organization of behavior was proposed by L.Kachalova.2 Based on the fact that parkinsonism doesaffect the programming level, but that there is a breakdoin the part of the motor plan that designates where and wa motion must be carried out, as well as based on the factaction is triggered by a goal and is made up of preparautomatic motor actions17 and that the sensory characteristiof the goal and the circumstances are unavoidably altewhen the action is implemented, i.e., the feedback for atrary motion includes not only signals from the musclesalso the current readings of the distance analyzers thatused as tracking systems in behavior, tuned to search forexpect information,1 she concluded that a mechanism is posible in accordance with which the CN has direct informatfrom the output~reverse motor afferentation! and directlyinfluences the input~projection to the analyzers!. Thus, alarge number of afferent cells from various levels of tbrain form an ‘‘integral’’ in the CN, which arrives simultaneously at the input and the output of the system: atanalyzers and the motor cortex. The object of the mosensory influence is the analyzers, and, as a result ofinfluence, the analyzers are used in behavior as trackingtems that ensure an arbitrary level of control, anticipatingadjustment regime and the coordination with the work ofskeletal musculature.

There are data showing that efferent copies that copletely correspond to the information arriving directly at tmotor neurons can enter the striopallidal system alonglaterals of the pyramidal tract. Similar copies enter the sthalamic nucleus, which is the key structure of the intertion of the pyramidal and the extrapyramidal systems anunder the direct monosynaptic influence of collaterals ofpyramidal tract.2 Most of the axons of the efferent neuronsthe subthallamic nucleus branch out to the globus palliand the substantia nigra. A system is thus organizedtakes into account not only kinetic influences but also mo

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afferentation of central origin, by means of which the sesory apparatus becomes capable of adjustment in a regimnot only current dynamics, but also of assumed motornamics; i.e., it can form an anticipatory pattern of behavioreaction.

We used mongrel dogs and lower primates~Macacarhesus! to study the restoration of pulse activity of the nerons of functionally different regions of the brain and theinterrelationships, which correlate with various phases ofconditioned-reflex behavior in unanesthetized animals.

It has been established that the head of the CN contcells that specifically react to spatial localization of signand their biological significance, altering their activity indefinite way during the formation of anticipatory excitatioassociation of conditioned and unconditioned excitants,decision making.

In order to explain the systemic mechanisms and theand sequence of switching on the neural formations ofcortex, the neostriatum, and the amygdala in the organizaof conditioned-reflex behavior in dogs, we studied the intaction of the activity of their neurons. By using croscorrelation analysis and by constructing cross-interval hisgrams, it was shown that there is no interaction in tbackground between the cells of learned structures. Infirst phase of the selection of a conditioned reflex, regardof the quality of the reaction of the neurons to presenconditioned and unconditioned signals, the connectionstween the head of the CN and the amygdala are initiastrengthened~a synchronized process is recorded 50–100earlier in the head of the CN! with a simultaneous but loweincrease of the functional coupling between the prefroncortex and the amygdala, and then~200–400 ms later! be-tween the head of the CN and the prefrontal cortex. Tsimplified conditional reflex is characterized by the appeance of a common process, most importantly in the prefrtal cortex, and then, with a lag of 50–100 ms, in tamygdala and in the head of the CN. A sharp decrease ocorrelation between the pulse activity of the neurons ofhead of the CN and of the amygdala is observed in tcase.5,7

The construction of bidirectional~in time! peristimulushistograms of the pulse activity of the cells in the head ofCN relative to the time of correct or incorrect pressureone of three keys~the solution of a problem on a deferrechoice! made it possible to reliably establish the variationthe activity of the neurons 300–600 ms after an incorrecchosen key relative to the activity of the neuron whenproblem is correctly solved~Fig. 1!. The histograms~Fig. 1!show time t on the horizontal axis and the numbern ofpulses in 200 ms on the vertical axis. At the vertical dottlines, the activity is synchronized relative to the instant ththe key is pressed. The horizontal dotted lines are the leof the mean frequency of the background pulsing; the blcolumns show the deviations of the pulse activity exceed2.58 G from the mean level. To construct each histogram,activity is summed for 8–10 implementations of each assiment.

In the numerous papers of K. B. Shapovalovaet al. onthe electrical stimulation of various sections of the head

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the CN, it was shown that, as the strength of the electraction increases, progressive breakdowns are observed iimplementation of motor programs all the way to the ‘‘cadate base’’—the complete instantaneous cessation of moregardless of what stage it has reached. Pharmacologication on the cholinergic system of the CN~see, for exampleRef. 4! causes a delay in the phase components of the hing of a raised paw at a definite level, which is evidencethe complete breakdown of the fine-tuning mechanism ocompleted motor program by means of reverse afferentat

Our own data and the literature data mentionabove5–7,10,11,18allow us to assume that information on thresult of cortical processes in the form of signals from stially and functionally different fields of the cortex and osubcortical structures, arriving at the CN, transforms thetivity of its cells in accordance with its specialization and,transforming itself in the neural network of the subcorticstructure, is converted into a new state of all the neuralments that reflects the state of the cortex and of the subtical structures as a whole. Commands to implement thesponse reaction also enter the CN along pyramidalextrapyramidal paths. Information concerning the ‘‘stadard’’ response that earlier produced the most efficientenergetically most favorable result enters the BG from strtures having a relation to memory processes—the amygand the hippocampus.~There is a widely known series ostudies6,10 that led to the assumption that the amygdala plan important role in the mechanism of long-term memorybiologically significant stimuli. It was shown in a numberpapers that destroying the amygdala can break down

FIG. 1. Peristimulus histograms of the pulse activity of a neuron ofcaudate nucleus for correct~left! and incorrect motor response at the timecarrying out various tasks on delayed spatial choice. See text for exption.

879 J. Opt. Technol. 66 (10), October 1999

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learning itself, but the transition from learning to executiobecause of the absence of its facilitating influence.11,18Com-binatorial analysis of the connections of the neostriatumthe primary inputs into the dorsal neostriatum from thefector structures and those into the ventral striatum fromstructures of the limbic system—presents a splendid pobility for the interaction of biologically different informationon the level of the BG.! Moreover, the BG obtain reversafferentation from all the effector organs concerning tcourse of the accomplishment of the program of the resporeaction. Starting from the principle of matched filtering,discrepancy of the accomplished program of behavior wthe result of reverse afferentation and prior experienshapes the command pulses of the efferent cells of the~Fig. 2!. For insignificant discrepancies, the resulting comand pulsing alters or modulates the command vector aring from the cortex.5 When the mismatch cannot be compesated, the carrying out of the program can be compleinhibited ~caudate shutdown, change of neural activity whone of the keys is chosen and pressed incorrectly!. Thus, oneof the main functions of the neostriatum is to generalizeresults of the specialized cortical analysis and the informtion from the subcortical structures and to use the princiof matched filtering to form command pulsing at the outpbecause the current and expected results of the actionhas been carried out do not match.

This work was carried out with the financial supportthe Russian Fund for Fundamental Research~Project Nos.97-04-49598 and 96-07-89112!.

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6N. F. Suvarov and V. T. Shuvaev, ‘‘Reconstruction of the activity of t

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FIG. 2. Diagram of the formation by the neostriatum of command pulswhen the completed behavioral program is mismatched with the datreverse afferentation and prior experience according to the principlematched filtering. See text for explanation.

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880V. T. Shuvaev