H. Q. Zhang

PARALLEL ORGANIZATION OF SOMATOSENSORY CORTICAL AREAS I AND II FOR TACTILE PROCESSING

1. The two principal tactile processing areas in the cerebral cortex, somatosensory areas I and II, receive direct projections from the thalamus and, as well, are linked through intracortical reciprocal connections. Tactile information may therefore be conveyed to SII, for example, over either a direct path from the thalamus or an indirect, or serial, path from the thalamus via SI.

Signalling of static and dynamic features of muscle spindle input by cuneate neurones in the cat

1 The capacity of cuneate neurones to signal information derived from muscle spindle afferent fibres about static stretch or vibration of forearm extensor muscles was examined electrophysiologically in anaesthetized cats. 2 Static stretch (<= 2 mm in amplitude) and sinusoidal vibration (at frequencies of 50‐800 Hz) were applied longitudinally to individual muscle tendons by means of a feedback controlled mechanical stimulator, and responses were recorded from individual cuneate neurones and from individual spindle afferent fibres. 3 Cuneate neurones sampled were located caudal to the obex and displayed a sensitivity to both vibration and static stretch of forearm muscles that was consistent with their input arising from primary spindle endings. In response to static muscle stretch, they displayed graded and approximately linear stimulus‐response relations, and a stability of response level at fixed lengths that was consistent with these neurones contributing discriminative information about static muscle stretch. 4 In response to sinusoidal muscle vibration the cuneate neurones also showed graded stimulus‐response relations (in contrast to spindle afferents which at low vibration amplitudes attain a plateau response level corresponding to a discharge of 1 impulse on each vibration cycle). Lowest thresholds were at 100‐300 Hz and bandwidths of vibration sensitivity extended up to ∼800 Hz. 5 Temporal precision in cuneate responses to muscle vibration was assessed by constructing phase scatter and cycle histograms from which measures of vector strength could be calculated. Cuneate responses displayed somewhat poorer phase locking (and lower vector strengths) than spindle afferent responses to vibration (a reflection of uncertainties associated with synaptic transmission). Nevertheless, the remarkable feature of cuneate responses to muscle vibration is the preservation of tight phase locking at frequencies up to 400‐500 Hz, which presumably enables these central neurones to contribute accurate temporal information for the kinaesthetic sense in a variety of circumstances involving dynamic perturbations to skeletal muscle.

Parallel organization of proprioceptive inputs from joint receptors to cortical somatosensory areas I and II in the cat.

1. Studies in monkeys indicate that proprioceptive and tactile inputs are conveyed from the thalamus to the primary somatosensory cortex (SI) and thence to the secondary somatosensory area (SII) in a serial scheme. In contrast, in the cat, tactile information is conveyed in parallel from the thalamus to SI and SII. The present study, in the cat, employed reversible inactivation of SI to determine whether proprioceptive inputs to SII from joint receptors depend on an indirect serial path via SI or are conveyed over a direct path from the thalamus. 2. SI and SII foci for knee joint inputs were determined with evoked potential mapping. Reversible inactivation of the SI focus by cooling had no effect on the amplitude, latency or time course of SII potentials evoked by joint inputs. There was also no consistent effect on the response levels of individual SII neurones examined during SI inactivation. Furthermore, there was no attenuation of the later components of the responses, and therefore no evidence that these depended on an indirect path to SII via SI. 3. Results demonstrate that proprioceptive inputs project directly from thalamus to SII over a pathway organized in parallel with that to SI, in contrast to the serial scheme reported for proprioceptive processing in primates.

Parallel processing in somatosensory areas I and II of the cerebral cortex

Somatosensory areas I and II (SI and SII) constitute two of the principal tactile processing areas in the cerebral cortex. They each receive direct projections from the thalamus and, as well, are linked through intracortical reciprocal connections. Tactile inputs may therefore be conveyed to SII, for example, over either a direct path from the thalamus or an indirect, or serial, path from the thalamus via SI. We have examined in the cat, rabbit and marmoset monkey the behaviour of SII neurons before, during and after the selective, rapidly-reversible inactivation of SI by means of localized cooling. The results demonstrate that in cat and rabbit, SII responsiveness is never abolished and infrequently affected by SI inactivation and that tactile inputs to SII therefore traverse a direct path from thalamus, organized in parallel with that to SI. In the marmoset (Callithrix jacchus), in contrast to earlier studies based on ablation of SI we found that with reversible inactivation of SI, SII responsiveness was unaffected in 25% of neurons and, although reduced in the remainder, was rarely abolished (<10% of SII neurons). The results indicate that there is substantial direct thalamic input to SII, even in this simian primate, and therefore necessitate revision of the hypothesis that tactile processing at the thalamocortical level in simian primates is based on a strict serial scheme in which tactile information is conveyed from the thalamus to SI and thence to SII.

Impulse propagation over tactile and kinaesthetic sensory axons to central target neurones of the cuneate nucleus in cat

Paired, simultaneous recordings were made in anaesthetized cats from the peripheral and central axons of individual tactile and kinaesthetic sensory fibres. The aim was to determine whether failure of spike propagation occurred at any of the three major axonal branch points in the path to their cuneate target neurones, and whether propagation failure may contribute, along with synaptic transmission failures, to limitations in transmission security observed for the cuneate synaptic relay. No evidence for propagation failure was found at the two major axonal branch points prior to the cuneate nucleus, namely, the T‐junction at the dorsal root ganglion, and the major branch point near the cord entry point, even for the highest impulse rates (∼400 impulses s−1) at which these fibres could be driven. However, at the highest impulse rates there was evidence at the central, intra‐cuneate recording site of switching between two states in the terminal axonal spike configuration. This appears to reflect a sporadic propagation failure into one of the terminal branches of the sensory axon. In conclusion, it appears that central impulse propagation over group II sensory axons occurs with complete security through branch points within the dorsal root ganglion and at the spinal cord entry zone. However, at high rates of afferent drive, terminal axonal propagation failure may contribute to the observed decline in transmission security within the cuneate synaptic relay.

An intact peripheral nerve preparation for examining the central actions of single kinaesthetic afferent fibres arising in the wrist joint of the cat

Intraneural microstimulation of single tactile or kinaesthetic afferent fibres arising in the hand of conscious human subjects has revealed marked differences among the different classes in their capacity to generate a perceptual response. In order to test the hypothesis that these different capacities might reflect a differential security in the transmission of singnals across synaptic junctions in the dorsal column nuclei or other levels of the somatosensory pathway we have previously developed a paired, simultaneous recording paradigm in the cat to analyze transmission characteristics within the dorsal column nuclei for single identified tactile and muscle sensory fibres of the forearm. These studies have depended upon the use of a fine peripheral nerve or nerve fascicle preparation in which it is possible to monitor the activity of single sensory fibres while the nerve remains in continuity with the central nervous system. Although we have previously described a preparation that allows the activity of single joint afferent fibres from the hindlimb to be monitored in the intact medial articular nerve, these hindlimb kinaesthetic afferents fail to project directly to the dorsal column nuclei. In the present study we report a forearm nerve preparation in the cat that permits the simultaneous recording of activity from individual wrist joint afferent fibres and their target neurones of the dorsal column nuclei. When this nerve is freed from nearby tissue over a distance of 2-4 cm and left in continuity, it is possible with a silver hook electrode to monitor the impulse activity of each group II joint afferent fibre with an excellent signal-to-noise ratio. The preparation should prove ideal for examining the central actions and security of transmission across the dorsal column nuclei for single, identified joint afferent fibres of the forearm.

An intact nerve preparation for monitoring inputs from single joint afferent fibres

A preparation is described that permits the monitoring of activity from individual joint afferent nerve fibres in an intact peripheral nerve of the cat. The joint nerve used was the medial articular nerve (MAN) that supplies the medial and anteromedial aspects of the knee joint. This nerve is sufficiently fine that if freed from nearby tissue over a length of 2-5 cm and placed over a platinum hook electrode it is possible to identify and monitor, from the intact nerve, the impulse activity from each group II joint afferent fibre activated by mechanical stimulation of the joint capsule. The signal-to-noise ratio exceeds 5:1 and in most cases was approximately 10:1. With this preparation it is now possible to examine the central actions and security of transmission at central synaptic targets for single, identified group II joint afferent fibres.

The effects of neonatal median nerve injury on the responsiveness of Tactile neurones within the cuneate nucleus of the cat

1 The capacity of cuneate neurones to attain normal functional properties following neonatal median nerve injury was investigated with single neurone recording in anaesthetized cats, 12–24 months subsequent to a controlled crush injury. Effectiveness of the peripheral nerve injury was confirmed by the abolition of the median nerve compound action potential following the crush. 2 Cuneate recording was carried out after denervation of the forearm, apart from the median nerve, to ensure that neurones studied had receptive fields within the distribution zone of the regenerated median nerve. Controlled and reproducible tactile stimuli were used to evaluate the functional capacities of neurones to determine whether they were consistent with those reported earlier for cuneate neurones in cats that had normal peripheral nerve development. 3 Twenty‐two cuneate neurones with well‐defined tactile receptive fields within the distribution zone of the regenerated median nerve were classified according to their adaptation characteristics and functional properties. Slowly adapting neurones responded throughout static skin indentations and had graded and approximately linear stimulus–response relations over indentation ranges up to 1.5 mm. Rapidly adapting neurones responded to the dynamic phases of skin indentations and could be divided into two broad classes, one most sensitive to vibrotactile stimuli at 200–400 Hz which appeared to receive a predominant input from Pacinian corpuscle receptors, and a non‐Pacinian group that included neurones most sensitive to skin vibration at 5–50 Hz which appeared to receive glabrous skin input from the rapidly adapting class of afferent fibres. 4 Based on the stimulus‐response relations and on measures of phase locking in the responses to vibrotactile stimuli, it appears that the functional properties of cuneate neurones activated from the field of a regenerated median nerve subsequent to a neonatal nerve crush injury were consistent with those reported previously for ‘control’ cuneate neurones. The results indicate that cuneate neurones can acquire normal tactile coding capacities despite the disruption caused by prior crush injury to their peripheral nerve source.