Peter Redgrave

The basal ganglia : a vertebrate solution to the selection problem?

A selection problem arises whenever two or more competing systems seek simultaneous access to a restricted resource. Consideration of several selection architectures suggests there are significant advantages for systems which incorporate a central switching mechanism. We propose that the vertebrate basal ganglia have evolved as a centralized selection device, specialized to resolve conflicts over access to limited motor and cognitive resources. Analysis of basal ganglia functional architecture and its position within a wider anatomical framework suggests it can satisfy many of the requirements expected of an efficient selection mechanism.

Goal-directed and habitual control in the basal ganglia: implications for Parkinson's disease

Progressive loss of the ascending dopaminergic projection in the basal ganglia is a fundamental pathological feature of Parkinsons disease. Studies in animals and humans have identified spatially segregated functional territories in the basal ganglia for the control of goal-directed and habitual actions. In patients with Parkinsons disease the loss of dopamine is predominantly in the posterior putamen, a region of the basal ganglia associated with the control of habitual behaviour. These patients may therefore be forced into a progressive reliance on the goal-directed mode of action control that is mediated by comparatively preserved processing in the rostromedial striatum. Thus, many of their behavioural difficulties may reflect a loss of normal automatic control owing to distorting output signals from habitual control circuits, which impede the expression of goal-directed action.

Subcortical loops through the basal ganglia

Parallel, largely segregated, closed-loop projections are an important component of cortical-basal ganglia-cortical connectional architecture. Here, we present the hypothesis that such loops involving the neocortex are neither novel nor the first evolutionary example of closed-loop architecture involving the basal ganglia. Specifically, we propose that a phylogenetically older, closed-loop series of subcortical connections exists between the basal ganglia and brainstem sensorimotor structures, a good example of which is the midbrain superior colliculus. Insofar as this organization represents a general feature of brain architecture, cortical and subcortical inputs to the basal ganglia might act independently, co-operatively or competitively to influence the mechanisms of action selection.

A computational model of action selection in the basal ganglia. II. Analysis and simulation of behaviour

Abstract. In a companion paper a new functional architecture was proposed for the basal ganglia based on the premise that these brain structures play a central role in behavioural action selection. The current paper quantitatively describes the properties of the model using analysis and simulation. The decomposition of the basal ganglia into selection and control pathways is supported in several ways. First, several elegant features are exposed – capacity scaling, enhanced selectivity and synergistic dopamine modulation – which might be expected to exist in a well designed action selection mechanism. The discovery of these features also lends support to the computational premise of selection that underpins our model. Second, good matches between model globus pallidus external segment output and globus pallidus internal segment and substantia nigra reticulata area output, and neurophysiological data, have been found which are indicative of common architectural features in the model and biological basal ganglia. Third, the behaviour of the model as a signal selection mechanism has parallels with some kinds of action selection observed in animals under various levels of dopaminergic modulation.

A direct projection from superior colliculus to substantia nigra for detecting salient visual events

Midbrain dopaminergic neurons respond to unexpected and biologically salient events, but little is known about the sensory systems underlying this response. Here we describe, in the rat, a direct projection from a primary visual structure, the midbrain superior colliculus (SC), to the substantia nigra pars compacta (SNc) where direct synaptic contacts are made with both dopaminergic and non-dopaminergic neurons. Complementary electrophysiological data reveal that short-latency visual responses in the SNc are abolished by ipsilateral lesions of the SC and increased by local collicular stimulation. These results show that the tectonigral projection is ideally located to relay short-latency visual information to dopamine-containing regions of the ventral midbrain. We conclude that it is within this afferent sensory circuitry that the critical perceptual discriminations that identify stimuli as both unpredicted and biologically salient are made.

Descending projections from the superior colliculus in rat: a study using orthograde transport of wheatgerm-agglutinin conjugated horseradish peroxidase

SummaryDespite extensive behavioural work on the rat superior colliculus, its descending efferent pathways have not been fully characterised with modern anatomical tract-tracing techniques. To investigate these pathways, wheatgerm-agglutinin conjugated with horseradish peroxidase (1%) was injected at various locations within the superior colliculus of hooded rats. Label judged to be transported orthogradely was plotted on coronal sections modified from the atlas of Paxinos and Watson (1982). Two major descending pathways were identified, (i) The bulk of the fibres in the ipsilateral descending pathway leave the superior colliculus ventrolaterally, and course around the lateral margin of the midbrain reticular formation. Caudally, projecting fibres leave the main bundle to innervate the cuneiform nucleus, and parts of the pontomedullary reticular formation. Terminal fields associated with the major bundle of fibres are found in an area medial to the brachium of the inferior colliculus; the parabigeminal nucleus and adjacent tegmentum; the ventrolateral midbrain reticular formation; and the lateral pontine nuclei, (ii) The fibres of the main contralateral descending pathway leave the superior colliculus ventromedially, to cross midline in the dorsal tegmental decussation. They immediately turn caudally to join the predorsal bundle, in which they run the length of the brainstem to reach the cervical spinal cord. Major terminal fields occur in nucleus reticularis tegmenti pontis; the pedunculopontine/ parabrachial area; paramedian pontomedullary reticular formation; and inferior olive. In addition there is lighter labelling in many areas of the pontomedullary reticular formation and in the cervical spinal cord. There was also a much sparser contralateral descending projection that crossed midline in the tectal commissure, and sent terminals to the contralateral cuneiform area and adjoining regions. These results suggest that the distribution of the descending efferent pathways from the superior colliculus in rats is similar to those described in other species. The fact that the two major pathways project to quite different terminal areas, together with previous findings that they have separate cells of origin within the tectum, suggests that they may also be functionally distinct.

Topographical organization of the nigrotectal projection in rat: Evidence for segregated channels

Recent evidence suggests that projections from the superior colliculus to the brainstem in rat are organized into a series of anatomically segregated output channels. To understand how collicular function may be modified by the basal ganglia it is important to know whether particular output modules of the superior colliculus can be selectively influenced by input from substantia nigra. The purpose of the present study was, therefore, to examine in more detail topography within the nigrotectal system in the rat. Small injections (10-50 nl) of a 1% solution of wheatgerm agglutinin conjugated with horseradish peroxidase were made at different locations within substantia nigra and surrounding structures. A discontinuous puff-like pattern of anterogradely transported label was found in medial and caudal parts of the ipsilateral intermediate layers of the superior colliculus. In contrast, the rostrolateral enlargement of the intermediate layers contained a greater density of more evenly distributed terminal label. Injection sites associated with this dense pattern of laterally located label were concentrated in lateral pars reticulata, while the puff-like pattern was produced by injections into ventromedial pars reticulata. Retrograde tracing experiments with the fluorescent dyes True Blue and Fast Blue revealed that injections involving the rostrolateral intermediate layers were consistently associated with a restricted column of labelled cells in the dorsolateral part of ipsilateral pars reticulata. Comparable injections into medial and caudal regions of the superior colliculus produced retrograde labelling in ventral and medial parts of the rostral two-thirds of pars reticulata. Both anterograde and retrograde tracing data indicated that contralateral nigrotectal projections arise from cells located in ventral and medial pars reticulata. The present results suggest that the main ipsilateral projection from substantia nigra pars reticulata to the superior colliculus comprises two main components characterized by regionally segregated populations of output cells and spatially separated zones of termination. Of particular interest is the apparent close alignment between terminal zones of the nigrotectal channels and previously defined populations of crossed descending output cells in the superior colliculus. Thus, the rostrolateral intermediate layers contain a concentration of terminals specifically from dorsolateral pars reticulata and output cells which project to the contralateral caudal medulla and spinal cord. Conversely, the medial and caudal intermediate layers receive terminals from ventral and medial pars reticulata and contain cells which project specifically to contralateral regions of the paramedian pontine and medullary reticular formation.(ABSTRACT TRUNCATED AT 400 WORDS)

Computational models of the basal ganglia: from robots to membranes

With the rapid accumulation of neuroscientific data comes a pressing need to develop models that can explain the computational processes performed by the basal ganglia. Relevant biological information spans a range of structural levels, from the activity of neuronal membranes to the role of the basal ganglia in overt behavioural control. This viewpoint presents a framework for understanding the aims, limitations and methods for testing of computational models across all structural levels. We identify distinct modelling strategies that can deliver important and complementary insights into the nature of problems the basal ganglia have evolved to solve, and describe methods that are used to solve them.

The hemodynamic impulse response to a single neural event.

This article investigates the relation between stimulus-evoked neural activity and cerebral hemodynamics. Specifically, the hypothesis is tested that hemodynamic responses can be modeled as a linear convolution of experimentally obtained measures of neural activity with a suitable hemodynamic impulse response function. To obtain a range of neural and hemodynamic responses, rat whisker pad was stimulated using brief (≤2 seconds) electrical stimuli consisting of single pulses (0.3 millisecond, 1.2 mA) combined both at different frequencies and in a paired-pulse design. Hemodynamic responses were measured using concurrent optical imaging spectroscopy and laser Doppler flowmetry, whereas neural responses were assessed through current source density analysis of multielectrode recordings from a single barrel. General linear modeling was used to deconvolve the hemodynamic impulse response to a single “neural event” from the hemodynamic and neural responses to stimulation. The model provided an excellent fit to the empirical data. The implications of these results for modeling schemes and for physiologic systems coupling neural and hemodynamic activity are discussed.

Output pathways from the rat superior colliculus mediating approach and avoidance have different sensory properties

SummaryNeuroanatomical studies have demonstrated that the two major descending pathways from the superior colliculus arise from regionally segregated, distinct, cells of origin. Stimulation and lesion studies have implicated the crossed descending tecto-reticulo-spinal projection in approach movements towards novel stimuli whereas the ipsilateral pathway appears to be involved in the control of avoidance and escape-like behaviours. The present electrophysiological study attempted to characterise the sensory properties of antidromically identified cells of origin of these pathways in anaesthetised rats. We found that the contralaterally projecting predorsal bundle (PDB) efferents were primarily somatosensory while the ipsilateral cuneiform (CNF) projection was primarily visual. PDB cells, mainly found in the intermediate layers, responded principally to vibrissal stimulation with their overlying visual fields optimally stimulated by small dark moving objects in the lower rostral and lateral field. In contrast, most CNF cells were located rostromedially, with the greatest contribution from visual cells responsive to stimuli in the upper rostral field. A significant proportion of these showed no response to small moving dark discs but fired vigorously to ‘looming’ stimuli. Ethological considerations suggest that these are appropriate stimulus characteristics for a system controlling approach and avoidance behaviour in an animal such as the rat where predators generally appear from above and prey is found on the ground.