Electrophysiological study of spinothalamic inputs to ventrolateral and adjacent thalamic nuclei of the cat

C. T. Yen, C. N. Honda, E. G. Jones

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Abstract

Extracellular and intracellular methods were used to record from fibers and neurons in the ventral lateral (VL) and adjacent nuclei of the cat thalamus. The receptive fields of the recorded units were analyzed and the units tested for inputs from the medial lemniscus (ML) and spinothalamic tract (STT) by electrical stimulation of the dorsal columns (DC) and ventrolateral funiculus (VLF) at the C2-3 spinal level. Thirty-eight STT fibers were isolated in the thalamus. Their conduction velocities ranged from 15 to 75 m/s (mode 36 m/s). Adequate stimuli were found for 23 of these fibers. Seventeen were low-threshold (LT), 3 were wide-dynamic-range (WDR), and 3 were high-threshold (HT) units. Five STT fibers were intra-axonally injected. Three were sufficiently well filled for analysis of their terminal fields. An intermediate-velocity STT fiber (conduction velocity 38 m/s) had a 4.3-μm axon and a single large terminal field in the central lateral nucleus (CL). The other two STT fibers were smaller, with diameters of 2.5 and 2.3 μm, conduction velocities of 15 and 19 m/s, and terminal fields made up of a few small boutons at the borders of the ventral posterior lateral nucleus (VPL). Of 319 neurons isolated, 14 out of 129 (10.8%) in VL, 14 out of 76 (18.4%) in the VPL or ventral posterior medial (VPM) nucleus, 27 out of 64 (42.2%) in the CL nucleus, and 5 out of 50 (10%) in the reticular nucleus (R) responded at latencies <50 ms to VLF stimuli. A train of three pulses was more effective in driving VLF-responding neurons in all these nuclei than a single pulse. VLF-responding cells were widely dispersed in VL, concentrated in a focus in CL, and distributed around the borders of VPL. Most of those in VL and a small number in CL could be antidromically activated by stimulation of motor cortex. Latencies of presynaptic responses (STT fibers) to VLF stimulation were short and varied from 0.8 to 3.9 ms (mode 1.6 ms). Despite this, very few fast-responding neurons were found. These were six VPL neurons (2.5 to 4 ms), one VL neuron (3 ms), and four CL neurons (3-4 ms). The initial spike latencies of the majority of thalamic neurons responding to VLF stimulation appeared in two peaks, one between 6 and 8 ms and the other at 10-15 ms. By contrast, responses of ML fibers to DC stimulation, even with a synaptic delay in the DC or lateral cervical nuclei, peaked at 2-4 ms, and many VPL neurons responded to DC stimulation with an initial spike latency <4 ms. Few or no neurons in the other nuclei had latencies ≤4 ms. The latencies of the small number of VL neurons responding to DC stimulation were ≥6 ms, implying polysynaptic activation. The shortest latencies of response of VL neurons to VLF stimulation included three recorded intracellularly, all showing initial excitatory postsynaptic potential latencies at 3 ms but initial spike latencies of 3, 7, and 9 ms. On the basis of the anatomic and electrophysiological data, therefore, it is likely that monosynaptic STT inputs to the individual thalamic cells studied are sparse and of low efficacy. Temporal summation is needed for activation in anesthetized animals. Even when activated, thalamic neurons show wide fluctuation in their spike latencies. Most of the isolated VL neurons responding to VLF stimulation could not be activated by natural stimuli. For the few neurons in which a receptive field was found, the adequate stimulus was usually slow and heavy tapping of the receptive field or occasionally intense pressure. These patterns of responsiveness were similar for CL neurons. A wider range of adequate stimuli was found for VPL neurons. Low-threshold units were found in the core of the VPL. Some of these units were inhibited by VLF stimuli. Excitatory VLF-responsive units were located at the borders of VPL. These neurons were either LT, WDR, or HT units. Some scattered R neurons also responded to these types of stimuli. Of the neurons responding to VLF stimulation at latencies <50 ms, 4/16 (25%) of the VL neurons, 9/57 (16%) of the VPL neurons, and 22/36 (61%) of the CL neurons showed convergent excitatory inputs from VLF and DC stimulation. A small number of R neurons (4/19, or 21%) also showed convergent inputs. The results show fundamental similarities between STT recipient neurons in the VL and CL and at the borders of the VPL nuclei. They confirm the general lack of direct DC inputs to VL neurons and suggest that STT inputs to VL neurons are unlikely to form a basis for the fast relay of light tactile and proprioceptive information to the motor cortex.

Original languageEnglish (US)
Pages (from-to)1033-1047
Number of pages15
JournalJournal of neurophysiology
Volume66
Issue number3
DOIs
StatePublished - 1991

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