Driss Boussaoud

Parietal inputs to dorsal versus ventral premotor areas in the macaque monkey: evidence for largely segregated visuomotor pathways.

The lateral premotor cortex plays a crucial role in visually guided limb movements. Visual information may reach this cortical region from the parietal cortex, the highest stage in the dorsal visual stream. Anatomical studies indicate that the parietal projections to the dorsal (PMd) and ventral (PMv) premotor areas arise from separate parietal regions, supporting the notion of parallel visuomotor pathways. We tested the degree of segregation of these pathways by injecting retrograde tracers into PMd and PMv in the same monkeys, under physiological control. Eleven injections were made in four animals, and the analysis of retrograde labelling revealed that parietal cells projecting to PMd and those projecting to PMv are largely segregated. The strongest projections to PMd arise from the superior parietal lobule, including the medial intraparietal area (MIP), PEc and PGm, and the parieto-occipital area. These areas were devoid of labelling following injections into PMv, which receives its major projections from the anterior intraparietal area (AIP), area PEip, the anterior portion of the inferior parietal gyrus (area 7b), and the somatosensory areas. In addition to their strong projections to PMv, areas 7b and PEip send minor projections to PMd as well. Additional projections to PMd arise from the ventral intraparietal area and the inferior parietal lobule. The present findings are direct anatomical evidence for largely segregated visuomotor pathways linking parietal cortex with PMd and PMv.

Direct visual pathways for reaching movements in the macaque monkey

The brain seems to process the location of objects faster than their intrinsic features, such as size, when these parameters are used to guide action. To uncover a potential anatomical substrate of these different processing speeds, we investigated in the monkey the pathways linking extrastriate visual cortex with the dorsal premotor area, a frontal area known to be involved in visually guided reaching movements. Retrogradely transported anatomical tracers were injected at physiologically defined sites and the distribution of labelled cells was examined in the ipsilateral cortex. We found a projection to the dorsal premotor cortex from the parieto-occipital area (PO). This area receives direct projections from the primary visual cortex (V1), and is part of the dorsal visual stream involved in the processing of spatial information. No direct projections to the dorsal premotor cortex arise from the ventral visual areas, thought to process object features. Our finding provides evidence for direct pathways from the dorsal visual stream to the dorsal premotor cortex and supports the view that the location of objects is processed faster by the brain than their intrinsic features.

Attention versus intention in the primate premotor cortex.

One challenging issue in cognitive neuroscience has been to dissociate a variety of mental processes from one another in order to elucidate brain functions. Attention, in particular, has been a recurrent issue because of its strong links with perceptual, cognitive, and motor performances. This paper reviews data from neurophysiological experiments designed to dissociate neuronal activity related to visuo-spatial attention from preparatory activity in the monkey brain. Cell activity was recorded from the dorsal premotor area (PMd) and compared to the dorsolateral prefrontal cortex (DLPf), from which it receives inputs. PMd has been implicated in the planing and execution of voluntary movements (PMd), and the majority of its cells are active during tasks with instructed delay time. However, the activity of many PMd cells is not specifically correlated with movement preparation, as is observed when the animal is attending to a visual stimulus, although the proportion of attention-related cells is much lower than in the DLPf. The distribution of attention-related and intention-related neurons within PMd tends to vary along the rostrocaudal axis, with the former more frequent rostrally (PMdr) and the latter more predominant caudally (PMdc). In a functional magnetic resonance imaging (fMRI) study in humans, we compared the premotor activation in two tasks: a spatial attention/memory task and a motor preparation task. The results suggest a rostrocaudal specialization within PMd of the human brain, with attention-related activation rostrally and medially and intention-related activation caudally. These studies indicate strong similarities in the functional organization of dorsal premotor cortex of human and monkey.

Effects of gaze on apparent visual responses of frontal cortex neurons.

Previous reports have argued that single neurons in the ventral premotor cortex of rhesus monkeys (PMv, the ventrolateral part of Brodmanns area 6) typically show spatial response fields that are independent of gaze angle. We reinvestigated this issue for PMv and also explored the adjacent prearcuate cortex (PAv, areas 12 and 45). Two rhesus monkeys were operantly conditioned to press a switch and maintain fixation on a small visual stimulus (0.2° × 0.2°) while a second visual stimulus (1° × 1° or 2° × 2°) appeared at one of several possible locations on a video screen. When the second stimulus dimmed, after an unpredictable period of 0.4–1.2s, the monkey had to quickly release the switch to receive liquid reinforcement. By presenting stimuli at fixed screen locations and varying the location of the fixation point, we could determine whether single neurons encode stimulus location in “absolute space” or any other coordinate system independent of gaze. For the vast majority of neurons in both PMv (90%) and PAv (94%), the apparent response to a stimulus at a given screen location varied significantly and dramatically with gaze angle. Thus, we found little evidence for gaze-independent activity in either PMv or PAv neurons. The present result in frontal cortex resembles that in posterior parietal cortex, where both retinal image location and eye position affect responsiveness to visual stimuli.

Subcortical connections of visual areas MST and FST in macaques

To examine the subcortical connections of the medial superior temporal and fundus of the superior temporal visual areas (MST and FST, respectively), we injected anterograde and retrograde tracers into 16 physiologically identified sites within the two areas in seven macaque monkeys. The subcortical connections of MST and FST were found to be very similar. Both areas were found to be reciprocally connected with the pulvinar, mainly with its medial subdivision, and with the claustrum. Nonreciprocal projections from both MST and FST were consistently found in the striatum (caudate and putamen), reticular nucleus of the thalamus, and the pontine nuclei. The labeled terminals in the pons were in the dorsolateral, lateral, dorsal, and peduncular nuclei. Additional nonreciprocal projections were found in one MST and one FST case to the nucleus of the optic tract, and, in one FST case, to the lateral terminal nucleus. Finally, three cases showed a nonreciprocal projection to FST from the basal forebrain. The subcortical structures containing label following MST and FST injections were largely the same as those labeled after injections of the middle temporal visual area (MT), but the label within each structure after MST and FST injections was more widespread than that from MT, overlapping the distribution of label that has been reported after injections of parietal visual areas. This finding is consistent with the known contributions of MST and FST to the functions of parietal cortex, such as eye-movement control.

High gamma frequency oscillatory activity dissociates attention from intention in the human premotor cortex

The premotor cortex is well known for its role in motor planning. In addition, recent studies have shown that it is also involved in nonmotor functions such as attention and memory, a notion derived from both animal neurophysiology and human functional imaging. The present study is an attempt to bridge the gap between these experimental techniques in the human brain, using a task initially designed to dissociate attention from intention in the monkey, and recently adapted for a functional magnetic resonance imaging (fMRI) study [Simon, S.R., Meunier, M., Piettre, L., Berardi, A.M., Segebarth, C.M., Boussaoud, D. (2002). Spatial attention and memory versus motor preparation: premotor cortex involvement as revealed by fMRI. J. Neurophysiol., 88, 2047-57]. Intracranial EEG was recorded from the cortical regions preferentially active in the spatial attention and/or working memory task and those involved in motor intention. The results show that, among the different intracranial EEG responses, only the high gamma frequency (60-200 Hz) oscillatory activity both dissociates attention/memory from motor intention and spatially colocalizes with the fMRI-identified premotor substrates of these two functions. This finding provides electrophysiological confirmation that the human premotor cortex is involved in spatial attention and/or working memory. Additionally, it provides timely support to the idea that high gamma frequency oscillations are involved in the cascade of neural processes underlying the hemodynamic responses measured with fMRI [Logothetis, N.K., Pauls, J., Augath, M., Trinath, T. and Oeltermann, A. (2001). Neurophysiological investigation of the basis of the fMRI signal. Nature, 412, 150-7], and suggests a functional selectivity of the gamma oscillations that could be critical for future EEG investigations, whether experimental or clinical.

Gaze effects in the cerebral cortex: reference frames for space coding and action

Abstract Visual information is mapped with respect to the retina within the early stages of the visual cortex. On the other hand, the brain has to achieve a representation of object location in a coordinate system that matches the reference frame used by the motor cortex to code reaching movement in space. The mechanism of the necessary coordinate transformation between the different frames of reference from the visual to the motor system as well as its localization within the cerebral cortex is still unclear. Coordinate transformation is traditionally described as a series of elementary computations along the visuomotor cortical pathways, and the motor system is thought to receive target information in a body-centered reference frame. However, neurons along these pathways have a number of similar properties and receive common input signals, suggesting that a non-retinocentric representation of object location in space might be available for sensory and motor purposes throughout the visuomotor pathway. This paper reviews recent findings showing that elementary input signals, such as retinal and eye position signals, reach the dorsal premotor cortex. We will also compare eye position effects in the premotor cortex with those described in the posterior parietal cortex. Our main thesis is that appropriate sensory input signals are distributed across the visuomotor continuum, and could potentially allow, in parallel, the emergence of multiple and task-dependent reference frames.

Frontal lobe mechanisms subserving vision-for-action versus vision-for-perception

In the typical course of daily events, we often gaze at an object, attend to its features and its place, reach toward it and grasp it, all with an awareness of what we are doing at the time. But behavior is not always thus. Gaze, attention, limb movement direction and awareness can be behaviorally dissociated from each other, and this review focuses on one such dissociation: that between the perception of an object and the use of that objects inherent spatial and nonspatial information for mediating visuomotor control. We review evidence that partially different neuronal systems underlie these two aspects of visual information processing. In neurophysiological studies of the primate frontal lobe, it has been possible to demonstrate that neural signals appearing to be visual responses reflect, at least in part, the motor significance of a stimulus. This finding has been confirmed, in separate studies, for both spatial and nonspatial visual information and supports the hypothesis that some frontal cortex activity reflects the selection and guidance of action rather than the properties of visual stimuli, per se. These findings are discussed in the context of neuropsychological studies indicating that accurate and appropriate movements are possible without perceptual awareness of the information guiding those movements.

Role of the cat substantia nigra pars reticulata in eye and head movements I. Neural activity

Summary1. Single unit activity was recorded in the Substantia Nigra pars reticulata (SNpr) of cats trained to orient their gaze toward visual and/or auditory targets. 2. Cells in the SNpr have a steady high rate of spontaneous activity ranging from 35 to 120 spikes per second. The neurons respond to sensory stimuli or in relation to saccadic eye movements with a decrease or a cut-off of the spontaneous discharge. 3. Among 109 cells recorded in the SNPR 60 were responsive to visual stimuli (mean latency = 118 ms). Most of the receptive fields which were plotted were large encompassing part of the ipsilateral field. 4. Thirty nine (39) cells were responsive to auditory stimuli (mean latency = 81 ms). A majority of these cells showed a better response for stimuli located in the contralateral hemifield. 5. In a few cells, the sensory responses were modulated by the subsequent orienting behavior of the animals. 6. Thirty one (31) cells showed a response in relation to saccades. These units typically stopped discharging between 50 and 300 ms prior to the onset of the saccade. 39% of these units also responded in relation to spontaneous saccades in the dark. 61% of the saccadic cells also responded to sensory stimuli in the absence of saccades. Six (6) cells were found to respond to active head movements. 7. These results are discussed in the framework of the role that the basal ganglia might have in the selection of the sensory stimuli that trigger orienting behaviors.

Origin of thalamic inputs to the primary, premotor, and supplementary motor cortical areas and to area 46 in macaque monkeys: A multiple retrograde tracing study

The origin of thalamic inputs to distinct motor cortical areas was established in five monkeys to determine whether the motor areas receive inputs from a common thalamic nucleus and the extent to which the territories of origin overlap. To not rely on the rough definition of cytoarchitectonic boundaries in the thalamus, monkeys were subjected to multiple injections of tracers (four to seven) in the primary (M1), premotor (PM), and supplementary (SMA) motor cortical areas and in area 46. The cortical areas were distributed into five groups, each receiving inputs from a specific set of thalamic nuclei: 1) M1; 2) SMA‐proper and the caudal part of the dorsal PM (PMdc); 3) the rostral and caudal parts of the ventral PM (PMvr and PMvc); 4) the rostral part of the dorsal PM (PMdr); and 5) the superior and inferior parts of area 46 (area 46sup and area 46inf). A major degree of overlap was obtained for the origins of the thalamocortical projections directed to areas 46inf and 46sup and for those terminating in SMA‐proper and PMdc. PMvc and PMvr received inputs from adjacent and/or common thalamic regions. In contrast, the degree of overlap between M1 and SMA was smaller. The projection to M1 shared relatively limited zones of origin with the projections directed to PM. Thalamic inputs to the motor cortical areas (M1, SMA, PMd, and PMv), in general, were segregated from those directed to area 46, except in the mediodorsal nucleus, in which there was clear overlap of the territories sending projections to area 46, SMA‐proper, and PMdc. J. Comp. Neurol. 409:131–152, 1999.