Cross-correlation analysis reveals laminar differences in thalamocortical interactions in the somatosensory system

Martha J. Johnson, Kevin D. Alloway

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Abstract

1. Spontaneous and stimulus-induced activity were recorded from corresponding somatotopic representations in the ventroposterolateral nucleus (VPL) of the thalamus and primary somatosensory (SI) cortex of intact, halothane-anesthetized cats. Thalamic and cortical neurons with overlapping receptive fields on the hairy skin of the forelimb were excited by a series of interleaved air jets aimed at multiple skin sites. 2. The laminar locations of 68% (240 of 355) of the neurons recorded in SI cortex were histologically reconstructed and responses of these 240 SI neurons were analyzed with respect to responses recorded from 118 thalamic neurons. Maximum responsiveness during the initial onset (1st 100 ms) of air jet stimulation was similar for neurons distributed throughout all layers of SI cortex (2-4 spikes per stimulus) and did not differ significantly from VPL responses. During the subsequent plateau phase of the stimulus. VPL neurons discharged at a mean rate of 19.0 spikes/s and neurons in cortical layers II, IIIa, IIIb, and IV discharged at similar rates. Mean responsiveness during the plateau phase of the stimulus was significantly reduced among neurons in conical layers V and VI and only averaged 7.1 and 3.9 spikes/s, respectively. 3. Responses recorded simultaneously from pairs of thalamic and cortical neurons were analyzed with cross-correlation analysis to determine differences in the incidence and strength of neuronal interactions as a function of cortical layer. Among 421 thalamocortical neuron pairs displaying stimulus-induced responses, 68 neuron pairs exhibited significant interactions during air jet stimulation. A laminar analysis revealed that 28% (45 of 163) of the neurons in the middle conical layers displayed significant interactions with thalamic neurons, whereas only 14% (13 of 92) of superficial layer neurons and 6% (10 of 166) of deep layer neurons were synchronized with thalamic activity during air jet stimulation. When thalamocortical efficacy for different layers of cortex was plotted as a cumulative frequency distribution, the strongest interactions in the middle cortical layers were twice as strong as interactions involving the superficial or deep cortical layers. 4. More than 70% of stimulus-induced interactions involved thalamic discharges followed by subsequent cortical discharges and the majority of these interactions involved interspike intervals of ≤ 3 ms. Nearly 75% (27 of 37) of interactions in the thalamocortical direction that involved cortical neurons in layers IIIb and IV transpired within a 3-ms interspike interval. For interactions with superficial or deep cortical layers, the proportion of thalamocortical interactions transpiring within 3 ms was only 58% (7 of 12) and 33% (2 of 6), respectively. 5. Cross correlation analysis of spontaneous activity indicated that 124 pairs of thalamic and conical neurons displayed synchronous activity in the absence of sensory stimulation. A laminar analysis indicated that similar proportions of cortical neurons in each layer were synchronized with thalamic activity in the absence of cutaneous stimulation. Thus 27% (44 of 163) of middle layer neurons, 30% (28 of 92) of superficial layer neurons, and 31% (51 of 166) of deep layer neurons displayed spontaneous interactions with thalamic neurons. The temporal pattern of spontaneous activity was examined with autocorrelation analysis to determine whether neuronal oscillations were essential for coordinating thalamic and cortical activity in the absence of peripheral stimulation. Only 18.5% (23 of 124) of spontaneous interactions between thalamic and cortical neurons were associated with periodic activity, which suggests that thalamocortical synchronization occurs before the constituent neurons begin to oscillate. 6. The influence of sensory stimulation on spontaneous interactions was examined in 31 pairs of thalamic and cortical neurons that exhibited interactions during prestimulus and stimulus intervals. A matched-sample analysis indicated that thalamocortical connection strength was significantly greater during cutaneous stimulation than during spontaneous activity. Further analysis of peak half-widths in the cross-correlograms also showed thai cutaneous stimulation produced significant decreases in the temporal variability of thalamocortical interactions. 7. These findings indicate that neurons in VPL have stronger functional connections with SI neurons in layers IIIb and IV than with neurons in other cortical layers. The relative incidence of interactions with neurons in superficial and deep cortical layers, together with laminar differences in the rate of stimulus-induced activity, suggests the presence of serial projections from middle to superficial layer neurons. These results are consistent with anatomic evidence, and the relationship between thalamocortical physiology and anatomy is discussed further in the text.

Original languageEnglish (US)
Pages (from-to)1444-1457
Number of pages14
JournalJournal of neurophysiology
Volume75
Issue number4
DOIs
Publication statusPublished - Jan 1 1996

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All Science Journal Classification (ASJC) codes

  • Neuroscience(all)
  • Physiology

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