Helen E. Savaki

Observation of action: grasping with the mind's hand☆

Engagement of the primary motor cortex (MI) during the observation of actions has been debated for a long time. In the present study, we used the quantitative 14C-deoxyglucose method in monkeys that either grasped 3-D objects or observed the same movements executed by humans. We found that the forelimb regions of the MI and the primary somatosensory (SI) cortex were significantly activated in both cases. Our study resolves a debate in the literature, providing strong evidence for use of MI representations during the observation of actions. It demonstrates that the observation of an action is represented in the primary motor and somatosensory cortices as is its execution. It indicates that in terms of neural correlates, recognizing a motor behavior is like executing the same behavior, requiring the involvement of a distributed system encompassing not only the premotor but also the primary motor cortex. We suggest that movements and their proprioceptive components are stored as motor and somatosensory representations in motor and somatosensory cortices, respectively, and that these representations are recalled during observation of an action.

When vision guides movement: a functional imaging study of the monkey brain

Goal-directed reaching requires a precise neural representation of the arm position and the target location. Parietal and frontal cortical areas rely on visual, somatosensory, and motor signals to guide the reaching arm to the desired position in space. To dissociate the regions processing these signals, we applied the quantitative [(14)C]-deoxyglucose method on monkeys reaching either in the light or in the dark. Nonvisual (somatosensory and memory-related) guidance of the arm, during reaching in the dark, induced activation of discrete regions in the parietal, premotor, and motor cortices. These included the dorsal part of the medial bank of the intraparietal sulcus, the ventral premotor area F4, the dorsal premotor area F2 below the superior precentral dimple, and the primary somatosensory and motor cortices. Additional parietal and premotor regions comprising the ventral intraparietal cortex, ventral premotor area F5, and the ventral part of dorsal premotor area F2 were activated by visual guidance of the arm during reaching in the light. This study provides evidence that different regions of the parieto-premotor circuit process the visual, somatosensory, and motor-memory-related signals which guide the moving arm.

Functional Metabolic Mapping of the Rat Brain during Unilateral Electrical Stimulation of the Subthalamic Nucleus

The alterations in local metabolic activity of several anatomically distinct brain areas were investigated by means of the quantitative autoradiographic 2-deoxy-D-[1-14C]glucose method in awake rats during unilateral electrical stimulation of the subthalamic nucleus (STH). Unilateral electrical stimulation of the STH induced local metabolic activation (by 70% as compared with the control group), as well as distal metabolic activations in the substantia nigra reticulata (by 34%), globus pallidus (by 19%), entopeduncular nucleus (by 18%), deep layers of the superior colliculi (by 15%), and parafascicular thalamic nucleus (by 18%), ipsilaterally to the stimulated side. The ventrolateral motor thalamic nucleus as well as the limbic components, posterior cingulate cortex, and anteroventral thalamic nucleus displayed bilateral metabolic activations (by 20–28%). These results indicate that, in addition to its known ipsilateral motor connections, each STH is functionally related to the limbic system bilaterally. It is suggested that the STH is a site where the central motor information is accessible to the limbic system. Quantitative image analysis of individual serial sections in the STH, substantia nigra, and globus pallidus revealed a consistent dorsoventral pattern of topographic interrelations. Stimulation of either the dorsal or the ventral subdivision of the STH induced always stronger activation in the dorsal compartment of the substantia nigra and in the ventral compartment of the globus pallidus. These results suggest that the earlier-described inversion of the dorsoventral functional correspondence between the substantia nigra and globus pallidus may be partly mediated via the subthalamic nerve cells projecting collateral axons to both these areas.

The intraparietal cortex: subregions involved in fixation, saccades, and in the visual and somatosensory guidance of reaching.

The functional activity of the intraparietal cortex was mapped with the [14C]deoxyglucose method in monkeys performing fixation of a central visual target, saccades to visual targets, reaching in the light during fixation of a central visual target, and acoustically triggered reaching in the dark while the eyes maintained a straight ahead direction. Different subregions of the intraparietal cortical area 7 were activated by fixation, saccades to visual targets, and acoustically triggered reaching in the dark. Subregions in the ventral part of the intraparietal cortex (around the fundus of the intraparietal sulcus) were activated only during reaching in the light, in which case visual information was available to guide the moving forelimb. In contrast, subregions in the dorsal part of the intraparietal cortical area 5 were activated during both reaching in the light and the dark, in which cases somatosensory information was the only one available in common. Thus, visual guidance of reaching is associated with the ventral intraparietal cortex, whereas somatosensory guidance, based on proprioceptive information about the current forelimb position, is associated with dorsal intraparietal area 5.

Metabolic activity pattern in the motor and somatosensory cortex of monkeys performing a visually guided reaching task with one forelimb

The [14C]deoxyglucose method was used to map the metabolic activity in the primary somatosensory and motor cortex in monkeys (Macaca nemestrina) performing a unimanual task. The task required visually guided reaching and target holding at a rate of about 10 movements per min. The entire dorsoventral extent of the cortical region lying between the posterior crown of the arcuate and the anterior crown of the intraparietal sulci was reconstructed on the sagittal plane, from horizontal sections aligned on the fundus of the central sulcus. The metabolic mapping of the control monkey demonstrated homogeneous activity all around the central sulcus, bilaterally. The mapped activity in the performing monkeys displayed two different patterns. The first pattern, contralateral to the moving forelimb, was characterized by several discrete regions of increased metabolic activity, which were symmetrically distributed in a mirror image fashion around the fundus of the central sulcus. These activated regions correspond to the lower body, forelimb, and mouth areas of representation of body parts in previously reported maps in primary motor and somatosensory cortical areas. The second activity pattern ipsilateral to the moving forelimb, displayed activated somatosensory and motor regions corresponding only to the lower body, and mouth representations. Our study provides a continuous, high resolution map of activity pattern in the entire primary motor and somatosensory cortices, which demonstrates that the reaching forelimb is controlled by a discrete subregion in the contralateral somatosensorimotor cortex, whereas other subregions of body representation are actively involved, bilaterally, during the performance of a relatively simple motor behaviour.

The place code of saccade metrics in the lateral bank of the intraparietal sulcus.

The lateral intraparietal area (LIP) of monkeys is known to participate in the guidance of rapid eye movements (saccades), but the means it uses to specify movement variables are poorly understood. To determine whether area LIP devotes neural space to encode saccade metrics spatially, we used the quantitative [14C]deoxyglucose method to obtain images of the distribution of metabolic activity in the intraparietal sulcus (IPs) of rhesus monkeys trained to repeatedly execute saccades of the same amplitude and direction for the duration of the experiment. Different monkeys were trained to perform saccades of different sizes and in different directions. A clear topography of saccade metrics was found in the cytoarchitectonically identified area LIP ventral (LIPv) contralateral to the direction of the eye movements. We demonstrate that the representation of the vertical meridian runs parallel to the fundus of the IPs and that it is not orthogonal to the representation of the horizontal meridian. Instead, the latter runs through the middle of LIPv parallel to its border with area LIP dorsal (LIPd). The upper part of oculomotor space is represented rostrally and dorsally relative to the horizontal meridian toward the LIPv–LIPd border, whereas the lower part of oculomotor space is represented caudally and ventrally toward the caudal edge of the IPs. Saccade amplitude is also represented in an orderly manner.

Saccade-Related Information in the Superior Temporal Motion Complex: Quantitative Functional Mapping in the Monkey

Although the role of the motion complex [cortical areas middle temporal (V5/MT), medial superior temporal (MST), and fundus of the superior temporal (FST)] in visual motion and smooth-pursuit eye movements is well understood, little is known about its involvement in rapid eye movements (saccades). To address this issue, we used the quantitative 14C-deoxyglucose method to obtain functional maps of the cerebral cortex lying in the superior temporal sulcus of rhesus monkeys executing saccades to visual targets and saccades to memorized targets in complete darkness. Fixational effects were observed in MT-foveal, FST, the anterior part of V4-transitional (V4t), and temporal-occipital areas. Saccades to memorized targets activated areas V5/MT, MST, and V4t, which were also activated for saccades to visual targets. Regions activated in the light and in the dark overlapped extensively. In addition, saccades to visual targets activated areas FST and the intermediate part of the polysensory temporal-parietal-occipital area. Cortical activity related to visually guided saccades could be explained, at least in part, by visual motion. Because only oculomotor signals can account for the equally robust activations induced by memory saccades in complete darkness, we suggest that areas V5/MT, MST, and V4t receive and/or process saccade-related oculomotor information.

Frontal cortical areas of the monkey brain engaged in reaching behavior: A 14C-deoxyglucose imaging study

The ((14)C)-deoxyglucose method was employed to study whether different areas of the primate frontal lobe are involved in different aspects of reaching behavior. To this end, we mapped the functional activity of the frontal motor cortical areas in three monkeys performing reaching movements with one forelimb. The first monkey had to capture a peripheral visual target with a saccade and a forelimb-reach together, the second monkey had to reach a peripheral visual target with one forelimb while fixating a central target, and the third one had to reach a peripheral memorized target with one forelimb in complete darkness while the eyes maintained a straight ahead direction. The extent and intensity of activations were compared to those of three respective control monkeys: a saccade-control, a fixation-control, and a dark-control. The primary somatosensory (S1) and motor (F1) forelimb representation, the S1- and F1-trunk representation, the F2-dimple region, areas F3-forelimb, F4, F5-bank of arcuate sulcus, F7-ridge, the dorsal bank of cingulate sulcus, and 24 c were activated in all reaching monkeys regardless of accompanying visual stimulation and oculomotor behavior. Interestingly, the S1-forelimb activation in the monkey reaching to memorized targets in complete darkness was more pronounced than that in the monkeys reaching to visual targets in the light, indicating that increased somatosensory processing compensates for the absence of visual feedback. On the other hand, areas F2-periarcuate, F5-convexity, F6, and 23 were preferentially activated by reaching to visual targets and remained unaffected during reaching to memorized targets when no visual feedback was available.

Bilateral cerebral metabolic effects of pharmacological manipulation of the substantia nigra in the rat : unilateral intranigral application of the inhibitory gabaA receptor agonist muscimol

Rates of cerebral glucose utilization were measured by means of the autoradiographic 2-deoxy-D[1-14C]glucose technique in the rat brain in order to determine the metabolic effects of unilateral intranigral application of the GABAA agonist muscimol upon the substantia nigra and its targets. Intranigral injection of 1.5 microliters 0.3 M muscimol (52 micrograms total dose) induced local metabolic activation in the injected substantia nigra reticulata (by 87% as compared to the control group), and distal metabolic depressions in the nucleus accumbens, striatum, globus pallidus and subthalamic nucleus only ipsilaterally to the injected nigra. The remaining basal ganglia components, including the substantia nigra compacta and the entopeduncular nucleus were bilaterally unaffected. Among the principal efferent projections of the substantia nigra reticulata, the ventromedial and centrolateral thalamic nuclei as well as the deep layers of the superior colliculi were metabolically depressed bilaterally, whereas the ventrolateral, parafascicular and mediodorsal thalamic nuclei as well as the pedunculopontine nucleus displayed metabolic depressions ipsilateral to the muscimol-injection nigra. The ventromedial and centrolateral thalamic nuclei were depressed by 41 and 42%, respectively, in the ipsilateral side, and by 30 and 26% in the contralateral side, when compared to the respective values of the control group of rats. Furthermore, unilateral intranigral injection of 0.3 M muscimol induced metabolic depressions in reticular, intralaminar and prefrontal thalamocortical areas mostly ipsilateral to the injected nigra, as well as in limbic areas bilaterally. It is suggested that the present findings are due to a postsynaptic effect of muscimol on the nigral GABAergic cells and to a consequent metabolic depression of the basal ganglia and associated thalamocortical areas, in contrast to an earlier suggested presynaptic nigral effect of lower doses of intranigrally injected muscimol which induced metabolic activations within the same network. This suggestion is further supported by the fact that intranigrally injected substrate P19 induced similar effects to those elicited by the lower doses of intranigral muscimol and opposite to those induced at present by the higher muscimol dose. Moreover, it is further substantiated that the nigrothalamic GABAergic system is responsible for considerable transfer of information from one substantia nigra reticulata to the ipsilateral basal ganglia and associated thalamocortical components as well as to bilateral motor, intralaminar and limbic areas.

Topography of Visuomotor Parameters in the Frontal and Premotor Eye Fields

To determine whether the periarcuate frontal cortex spatially encodes visual and oculomotor parameters, we trained monkeys to repeatedly execute saccades of the same amplitude and direction toward visual targets and we obtained quantitative images of the distribution of metabolic activity in 2D flattened reconstructions of the arcuate sulcus (As) and prearcuate convexity. We found two topographic maps of contraversive saccades to visual targets, separated by a region representing the vertical meridian: the first region straddled the fundus of the As and occupied areas 44 and 6-ventral, whereas the second one occupied areas 8A and 45 in the anterior bank of the As and the prearcuate convexity. The representation of the vertical meridian runs along the posterior borders of areas 8A and 45 (deep in the As). In both maps, the upper part of visuo-oculomotor space is represented ventrally and laterally and the lower part dorsally and medially whereas dorsal and ventral regions are separated by the representation of the horizontal meridian.