Selection of actions in the basal ganglia–thalamocortical circuits: review and model
Introduction
We live in an overwhelmingly complex world in which many events occur simultaneously and which interacts in many different ways with ourselves, who in turn constantly move, orient to and manipulate objects in this external world. For providing coherent, goal directed behavior, i.e. for coordinating sensory information flow and motor activity and integrating them into a single perceptual-motor act, the brain seems to employ higher-level control operations. In this paper these operations will be referred to as selection processes.
In the sensory domain, the selection process is associated with attention or attentional set, i.e. a preferential processing of a selected source of sensory information in an environment containing multiple channels of information (Moray, 1970; Allport, 1980; Woods, 1990). The selection process in the motor domain is associated with motor preparatory set, i.e. preparing for a selected movement while suppressing the other movements (see review see Evarts et al. 1984). To emphasize the higher control of movement, the term voluntary (vs. reflexive) movement is used (Passingham, 1993). We believe that selection operations are not limited by sensory or motor domains, they are expressed as integral parts of the whole range of human behavior. The ability to select an appropriate action at a given time interval determines cognitive functions of the human brain.
Models of attention proposed over the last 50 years have been based on psychological, neuropsychological and, more recently, on ERP (event-related potentials) and PET (positron-emission tomography) studies. Reviewing all these models is beyond the scope of the paper. However, several insights presented in the literature on attention have had a strong impact on our own views and need to be briefly mentioned here. The most important of these insights are: (1) a notion of cognitive structures (anticipatory schemata) that prepare the perceiver to accept the information selected (Neisser, 1976); (2) a notion of an automatic mismatch operation in the pre-attention mode (Näätänen and Michie, 1979; Näätänen, 1992); (3) a scheme for attentional networks that includes different cortical and subcortical components implementing engage, disengage and shifting operations (Posner and Dehaene, 1994); (4) a parasol metaphor emphasising the active suppression of irrelevant sources of information in the attention mode (Woods, 1990); (5) a notion of the functional system that is constructed in the brain for achieving a certain goal (Anokhin, 1973); (6) the theory of neuronal group selection introduced to describe principles of brain functioning (Edelman, 1987); (7) the searchlight hypothesis articulated to explain the role of the thalamus in attention and consciousness (Skinner and Yingling, 1977; Crick, 1984; Koch and Crick, 1994); and (8) a hypothesis of synchronous large-scale behavior of neural networks proposed to explain how the brain combines different sensory features into a single percept (von der Malsburg and Schneider, 1986; Gray et al., 1990; Engel et al., 1992).
Models explaining the mechanisms of motor control and motor learning have been mainly based on neurophysiological and neuropsychological data. Almost all of them include the basal ganglia–thalamocortical circuits now viewed by a majority of researchers as parallel feed back loops with separate elements in the striatum, the pallidum, the substantia nigra and the thalamus. Although the exact functions of these circuits are still unknown, single unit recordings in these structures indicate that they are involved in preparation for and initiation of internally generated movements (Alexander et al., 1986; DeLong et al., 1992). Several hypotheses on the role of the basal ganglia in organization of behavior have been suggested emphasizing the involvement in different functions, such as in running the sequences of motor programs to complete a motor plan (Mardsen, 1982), in the process of motor learning (procedural memory) (Hikosaka, 1993), in the image forming operation which control the cortical image to drive (Tamai, 1996), in the initiation of movement in a behavioral context-dependent manner (Kimura, 1995), in learning an association between divergent stimuli for the initiation of sequences of movements (Rolls, 1994), in control of polysensory information to the cortex (McKenzie, 1984) and some other hypothetical functions.
During the last two decades in our laboratory at the Institute of the Human Brain in St Petersburg, we have used a unique opportunity for recording impulse activity of neurons and local field potentials from electrodes located in different parts of the basal ganglia, the thalamus and the cortical areas connected to these subcortical structures. The electrodes were implanted for diagnosis and therapy for Parkinsonian patients, patients with obsessive–compulsive disorder and epileptic patients. These people were those informed and consenting patients who remained unresponsive to all conventional forms of treatment and who were recommended by a special commission for stereotactic neurosurgery. The patients voluntarily participated in our investigations, having given written consent.
Several different behavioral tasks were devised to study sensory, motor and cognitive functions. Functional profiles of the evoked responses together with anatomical information were used for identification of electrodes' respective positions. These studies have been published in different Russian journals (Human Physiology, Sensory Systems, Journal of Higher Nervous Activity, I.M. Sechenov Physiological Journal) as well as in different international journals (International Journal of Psychophysiology, Journal of EEG and Clinical Neurophysiology, Psychophysiology). All these results, when put together, reveal a rather lucid and comprehensive picture of the functional features of the basal ganglia–thalamic circuits indicating their involvement in attention and motor preparation. Moreover, a single neurophysiological mechanism for implementing these functions can be proposed.
The goals of this paper are twofold: (1) to review the results of our own recording of impulse activity of neurons in Parkinsonian patients with implanted electrodes and to show the involvement of the subcortical structures in attention and motor preparation; and (2) to suggest a cortico-subcortical mechanism for the selection of actions (including sensory, motor and cognitive acts).
Section snippets
Experimental approach to study selection operations
To study the neurophysiological basis of selection processes a stimulus–response paradigm is often used. In this paradigm, stimuli from one or several different sources are presented for short intervals while a subject (an animal or a human being) is required to respond to them selectively in a certain way. The nature of the response is determined by the animal's previous classical conditioning or by verbal instruction to human volunteers. We want to stress from the onset that the
Reviewing own experimental findings
During the last 20 years, seven different versions of the stimulus-response paradigm were used in our laboratory to study sensory, motor and cognitive functions of the brain. Only five of them, that yielded the most insightful results, will be discussed on the present review. The electrodes were gathered together in bundles of six single 0.1 mm diameter wires insulated by a phtoroplast film, their tips separated from each other by 3 mm. In Parkinsonian patients, the sites targeted were
Reviewing clinical observations: impairment of selection operations in the basal ganglia diseases
As was shown in the previous section, our intracranial recording indicate the involvement of the basal ganglia in selection operations. This section deals with clinical observations that we found in literature. The full review of the basal ganglia diseases is beyond the scope of the present paper (for review see Sano et al., 1996; Wichmann and DeLong, 1996). Here we focus on only the clinical facts that indicate the impairment of selection processes in the basal ganglia diseases.
It should be
Need for a model
The basal ganglia still remain the most mysterious parts of the human brain. Many functions were ascribed to them starting from pure motor control to more complex cognitive function. Each of these suggested functions was based on a certain set of experimental data. The methods varied from recording neuronal reactions in behavioral monkey to reaction time measurement in PD patients with different level of medication.
It is quite obvious that a separate method can open only a small `window' to
Action
Action seems to be the most critical concept for understanding the brain functioning in general and the basal ganglia function in particular. The idea of action as a general description of assessment, cognitive and motor act comes from our observation that all these different acts are represented and spatially separated within the basal ganglia. The idea of action is actually an extension of Neisser's hypothetical anticipatory structures, called schemata. According to Neisser's postulate,
The hypothesis of action programming: general description
After introducing the theoretical concept of action the hypothesis of action can be formulated. While human behavior is divided into different actions, states of memorizing their results and states of preparation for actions, the brain in turn is divided into separate systems playing different roles in the organization of actions. The roles mediated by these systems are: (1) the selection, initiation, preparation, and suppression of actions (taken together these particular functions are
Mapping scheme vs. funneling and segregating circuits
Let us start the description of the system for action selection by analyzing the anatomical structure and function of the basal ganglia–thalamocortical circuits. So far, two quite opposite schemes of information flow within these circuits have been proposed. They are funneling (Percheron and Filion, 1991) and segregating (Alexander et al., 1986) schemes (for a review of connections of the basal ganglia see Parent, 1990; Gerfen, 1992). Ten years ago, the basal ganglia were considered to be, in
Acknowledgements
We thank Natalia P. Bechtereva for insightful discussions. This study was supported by the Austro-Russian Cultural Exchange Program OST-West Projekt 81 (GZ 45.300/1-IV/6a/93-96) and by grants given by the Russian Science Foundation (96-04-50560) and the Russian Humanitarian Science Foundation (97-06-08112) to the Russian laboratory.
References (98)
- et al.
Brain mechanisms of selective listening reflected by event-related potentials
Electroenceph. Clin. Neurophysiol.
(1987) - et al.
Neurophysiological correlates of visual stimulus recognition in man
Int. J. Psychophysiol.
(1984) - et al.
Human thalamic and pallidal neuronal responses to visual stimuli in a threshold recognition task
Electroenceph. Clin. Neurophysiol.
(1989) - et al.
In search of cerebral error detector
Int. J. Psychophysiol.
(1990) - et al.
Disinhibition as a basic process in the expression of striatal functions
TINS
(1990) - et al.
Wave form and neuronal mechanisms of the decision P350 elicited without pre-stimulus CNV or readiness potential in random sequences of near-threshold auditory clicks and finger stimuli
Electroenceph. Clin. Neurophysiol.
(1979) - et al.
Concurrent processing streams in monkey visual cortex
TINS
(1988) - et al.
The hippocampus — What does it do?
Behav. Neural Biol.
(1992) - et al.
Temporal coding in the visual cortex; new vistas on integration in the nervous system
TINS
(1992) - et al.
Potential related to go/no-go hand movement task with color discrimination in human
Neurosci. Lett.
(1989)
The neostrital mosaic: multiple levels of compartmental organization
TINS
New frontiers in the basal ganglia research
TINS
Endogenous brain potentials associated with selective auditory attention
Electroencephalog. Clin. Neurophysiol.
Striatal interneurons: chemical, physiological and morphological characterization
TINS
Role of basal ganglia in behavioral learning
Neurosci. Res.
Subcortical neuronal correlates of component P300 in man
Electroenceph. Clin. Neurophysiol.
Human depth ERP in a visual threshold recognition task
Electroenceph. Clin. Neurophysiol.
Event-related neuronal responses in the human strio-pallido-thalamic system. 1. Sensory and motor functions
Electroenceph. Clin. Neurophysiol.
Event-related neuronal responses in the human strio-pallido-thalamic system. 2. Cognitive functions
Electroenceph. Clin. Neurophysiol.
Caudate unit activity during operant feeding behavior in monkeys and modulation by cooling prefrontal cortex
Behav. Brain Res.
Early selective attention effects on the evoked potential. A critical review and reinterpretation
Biol. Psychol.
Extrinsic connections of the basal ganglia
TINS
Parallel processing in the basal ganglia: up to a point
TINS
ERPs to response production and inhibition
Electroenceph. Clin. Neurophysiol.
Attentional networks
TINS
Mapping P300 waves onto inhibition: Go/No-Go discrimination
Electroenceph. Clin. Neurophysiol.
Responses of striatal neurons in the behaving monkey. I. Head of the caudate nucleus
Behav. Brain Res.
The scalp topography of potentials in auditory and visual discrimination tasks
EEG Clin. Neurophysiol.
Memory: brain systems and behavior
TINS
A proposed reorganization of the cortical input-output system
Prog. Brain Res.
Subcortical correlates of the P300 potential complex to auditory stimuli
Electroenceph. Clin. Neurophysiol.
Functional and pathophysiological models of the basal ganglia
Curr. Opin. Neurobiol.
A subcortical correlate of P300 in man
Electroencephalog. Clin. Neurophysiol.
The subcortical dementia of supranuclear palsy
J. Neurol. Neurosurg. Psychiatr.
Functional architecture of basal ganglia circuits: neural substrates of parallel processing
TINS
Parallel organization of functionally segregated circuits linking basal ganglia and cortex
Ann. Rev. Neurosci.
Neurons — error detectors in subcortical structures of the human brain
Doklady Biol. Sci.
The behavioural and motor consequences of focal lesions of the basal ganglia in man
Brain
Function of the thalamic reticular complex: The searchlight hypothesis
Proc. Natl. Acad. Sci. USA
Vascular subcortical dementias: clinical aspects
Dementia
Is the P300 component a manifestation of context updating?
Behav. Brain Sci.
The Simon effect and attention deficits in Gilles de la Tourette's syndrome and Huntington's disease
Brain
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