We have recorded from 306 neurons in the inferior olive of six alert cats. Most of the cats were trained to perform a simple task with the forelimb. We observed the neural responses to a wide variety of cutaneous and proprioceptive stimuli, as well as responses during spontaneous and learned active movements. Neurons responsive to somatosensory stimulation were found in all parts of the inferior olive, and they were roughly evenly divided between those responsive to cutaneous stimulation and those responsive to proprioceptive stimulation. In the dorsal accessory olive all neurons were responsive to somatosensory stimulation. In the medial accessory nucleus 88% and in the principal olive 74% of cells were responsive to somatosensory stimulation. Cells responsive to cutaneous stimulation usually had small receptive fields, commonly on the paw. These cells had low-threshold responses to one or more forms of cutaneous stimulation and typically fired one spike at the onset of the stimulus on 80% or more of stimulus applications. Cells responsive to proprioceptive stimulation most commonly responded to passive displacements of a limb. These cells were often very sensitive, responding to linear displacements of less than 1 cm in one specific direction. No cells in our sample responded reliably during active movement by the animal. Only 21% of cells responding to passive proprioceptive stimulation showed any modulation during active movement, and the modulation was weak. Likewise, cells responsive to cutaneous stimulation generally failed to respond when a similar stimulus was produced by an active movement by the animal. Exceptions to this were stimuli produced during exploratory movements or when the receptive field unexpectedly made contact with an object during active movement. Electrical stimulation applied in the inferior olive failed to evoke movements or to modify ongoing movement. Our results are consistent with the hypothesis that inferior olivary neurons function as somatic event detectors responding particularly reliably to unexpected stimuli.

1. The primary goal of this study was to characterize the information about single-joint forelimb movements supplied to intermediate cerebellar cortex by mossy fibers. Discharge of mossy fibers and Golgi cells was studied while monkeys operated six devices that required movements about specific joints. Additional control experiments in anesthetized cats and monkeys established criteria for identification of mossy fibers and Golgi cells. 2. The control experiments demonstrate that mossy fibers can be distinguished from Purkinje and Golgi cells by the waveshapes of their action potentials. Asynaptic activation from the inferior cerebellar peduncle, in combination with histological localization of recording sites in granular layer or subcortical white matter, verified that mossy fibers produce a variety of waveshapes that are characterized by brief initial phases and relatively small amplitudes. The same waveshapes were observed for the mossy fiber recordings from awake monkeys, and many identified mossy fibers had sensory properties similar to those found in the awake animals. From these combined criteria, we conclude that the recordings in the awake animals were from mossy fibers. Golgi cells, recorded exclusively in the granular layer of cerebellar cortex, were characterized by action potentials of longer duration and larger amplitude as compared with mossy fibers, and none were asynaptically activated from the inferior cerebellar peduncle. 3. Units were isolated while the monkeys made free-form and tracking movements. We studied movement-related discharge of 80 mossy fibers and 12 Golgi cells. Mossy fibers showed high modulations during use of at least one of the six manipulanda and had clear preferences for movement about a specific joint, although they often showed consistent but weaker firing during movement about a neighboring joint. Separation of movements by more than one joint produced a large reduction in discharge: shoulder units never fired well to movements of the finger, and finger units never fired well to movement of the shoulder. 4. The tracking task required maintenance of fixed limb positions (a static phase) as well as movements between these positions (a dynamic phase). Of 80 mossy fibers, 18% had purely tonic discharge patterns, 63% were phasic-tonic, and 20% were purely phasic. Discharge patterns were reciprocal (45%), bidirectional (42%), or unidirectional (13%). 5. Eighty percent of the mossy fibers exhibited tonic discharge that was significantly (P < 0.01) correlated with joint angle (r = 0.65 +/- 0.19, mean +/- SD), and about one third had phasic components that were significantly correlated with movement velocity.(ABSTRACT TRUNCATED AT 400 WORDS)

No abstract

We examined the somatosensory properties of 391 neurons in the inferior olive in 20 cats that were anesthetized with barbiturate or decerebrated. A response consisted of a single spike with a variable number of wavelets followed by a long refractory period. Neurons responsive to natural somatosensory stimuli were recorded in all olivary subdivisions. The dorsal accessory olive (DAO) contained the highest proportion of responsive units (96%), compared with 66% for the medial accessory olive (MAO) and 43% for the principal olivary (PO) nucleus. Within the rostral DAO we found a refined cutaneous map of the entire contralateral body surface. In the caudal DAO responsiveness to manipulation of deep tissues became prominent, and both individual limbs and bilateral pairs were represented. In the medial region of the PO responsiveness to taps predominated and bilaterally symmetrical fields were frequent. The lateral PO was unresponsive under the conditions of these experiments. The MAO was distinguished by a greater complexity of receptive field and by a preponderance of deep over cutaneous modality. The lateral part of caudal MAO contained cells with interesting spatial patterns of excitation and inhibition, whereas most cells in the rostral MAO had purely excitatory fields. A teleceptive area receiving visual and auditory input was recognized in the medial MAO and nearby structures such as the dorsal cap. Contact and proprioceptive signals arriving via climbing fibers may provide the cerebellum with information necessary to relate the body to external objects.

1. The goal of this study was to investigate the motor organization of monkey nucleus interpositus (NI) and neighboring regions of the lateral nucleus (NL) by correlating discharge of single neurons with active movements. Neurons were surveyed during free-form movements as well as during operation of six devices that required movement about specific forelimb joints. The paradigm allowed us to test the hypothesis that discharge of individual cells relates to movements about individual joints. 2. One hundred sixty-two isolated nuclear neurons from two monkeys were studied. Eighty-three percent showed large increases in discharge (an average of 3 times resting rate for forelimb neurons) during movement of one body part, either forelimb, hindlimb, mouth/face, or eyes. 3. Anterior interpositus contains neurons related to hindlimb movement in anterior regions and neurons related to forelimb movement in posterior regions. A mouth/face-related area exists in the dorsal-posterior regions and is continuous with a mouth/face area in the dorsal regions of NL. Posterior interpositus (NIP) showed no clear separation between forelimb and hindlimb neurons: forelimb neurons were encountered throughout the nucleus, and hindlimb neurons were encountered in the medial-anterior two thirds. A distinct eye movement area exists in lateral, posterior, and ventral regions of NIP. This area borders regions of NL that also contain eye movement-related neurons. 4. Forelimb interpositus neurons discharged strongly during reach and grasp; discharge rates were recorded for 41 neurons during a stereotyped reach and the average depth of modulation was 149 imp/s. Nineteen neurons that modulated during device tracking were also tested during reaching, and the depth of modulation was much greater during reaching. 5. Fifty-nine forelimb neurons were tested with device tracking. Twenty-seven (46%) produced no audible modulation, regardless of the joint being exercised. The remaining 32 neurons modulated during movement on at least one device (mean depth of modulation = 84 imp/s). Comparison of discharge during use of different devices revealed no strong evidence for device-specific discharge. 6. Discharge modulations during device tracking were phasic, preceded movement, and, for a small number of cells, showed consistent parametric relations to duration, amplitude, and velocity of movement. 7. Despite a clear somatotopy within NI and NL, there is no finer mapping based on active movements about individual joints within forelimb regions. Discharge modulation depends on movements involving the whole limb. Progress in understanding the function of intermediate cerebellum depends on determining the variables required to elicit consistent and high modulation of neural discharge.(ABSTRACT TRUNCATED AT 400 WORDS)