The Anatomy of Manual Dexterity

1. 1 Purpose and Plan of This Review This review is focused on the topography and connections of some of the neuron populations that determine the manual dexterity of the macaque monkey. The populations selected for examination are the following: 1. The corticospinal neuron populations 2. The thalamocortical and corticothalamic neuron populations associated with the sensorimotor cortex 3. The ipsilateral cortical connections of the sensorimotor cortex These neuron populations have been chosen because of their obvious rel evance to the directed, intelligent use of the hands, but also because of their anatomical and functional interdependence. Corticospinal neuron populations transmit a complex, orchestrated output from a number of different regions of cerebral cortex to the neuron populations in every segment of the spinal cord, and this output includes the command information defining the intended manual action. The thalamocortical complex is especially concerned with the transmis sion and modulation or filtering of (a) visual, tactile, proprioceptive, vestibular, and auditory information to the cerebral cortex and (b) information from the cerebellum, basal ganglia, limbic system, and brain stem which is relevant to sensorimotor behavior. Finally, the extensive ipsilateral cortical connections constitute a major part of the supraspinal circuitry which coordinates the contri butions of all the cortical neuron popUlations contributing to intelligent sen sorimotor behavior and, in particular, transmits the cross talk between those cortical neuron populations which shape and control the dextrous handling of objects within reach.

The macaque monkey uses the hand to grasp, digitally explore, and identify objects within reach, and to use them intelligently. This review is focused on the topography and connections of some of the neuron populations that determine this manual dexterity. In the last decade these neuron populations have been analyzed using modern axon tracer techniques, single neuron recording in the alert monkey, and PET, resulting in a serious reconsideration of their structural and functional organization, and their roles in voluntary action. This review critically examines some of the new ideas triggered by these observations.

This review is focused on the topography and connections of some of the neuron populations that determine the manual dexterity of the macaque monkey. These neuron populations have been chosen because of their obvious relevance to the direct, intelligent use of the hands, but also because of their anatomical and functional interdependence.

1 Introduction.- 1.1 Purpose and Plan of This Review.- 1.2 Primate Manual Dexterity.- 2 Corticospinal Connections in the Primate.- 2.1 Introduction.- 2.2 New Methods.- 2.3 Direct Corticospinal Projections.- 2.4 Morphology of Corticospinal Neurons.- 2.5 Indirect Corticospinal Projections.- 2.6 Spinal Circuitry Mediating Supraspinal Control of Movement.- 2.7 Postnatal Maturation of Corticospinal Pathways.- 2.8 Comment.- 3 The Primate Sensorimotor Thalamus.- 3.1 The Thalamus and Sensorimotor Behavior.- 3.2 Architecture of the Dorsal Thalamus.- 3.3 Functional Groupings of Nuclei Within the Sensorimotor Thalamus.- 3.4 Thalamocortical Neuron Populations of the Sensorimotor Thalamus.- 3.5 Neuron Circuitry of Sensorimotor Thalamic Nuclei in the Macaque.- 3.6 The Pulvinar, Visually Directed Hand Movements, and Object Recognition.- 3.7 Comment.- 4 Sensorimotor Cortex.- 4.1 Introduction.- 4.2 Distribution of Visual Information in the Parietotemporal Cortex.- 4.3 Flow of Somatosensory Information in the Parietal Cortex in the Macaque.- 4.4 Visual Space, Tangible Space, and Their Neuronal Alignment.- 4.5 Connections Between Parietotemporal, Cingulate, and Prefrontal Cortex.- 4.6 Cortical Connections of Corticospinal Neuron Populations.- 5 Summary and Comments.- 6 References.- 7 Subject Index.