Effects of cortical stimulation on auditory-responsive thalamic neurones in anaesthetized guinea pigs

Abstract

In the present study, we investigated neuronal responses to acoustic stimuli and cortical stimulation in the medial geniculate body (MGB) through in vivo intracellular recordings in anaesthetized guinea pigs. Of the 54 neurones examined with acoustic stimuli, 36 showed excitatory postsynaptic potential (EPSP) responses and 19 showed inhibitory postsynaptic potential (IPSP) responses to acoustic stimuli. Of the 36 EPSP neurones examined with corticofugal modulation, 29 received corticofugal depolarization, 3 corticofugal inhibition, and 4 showed no effect. Of the 19 IPSP neurones, 17 received corticofugal inhibition and 2 were not affected. The mean amplitude of the EPSPs evoked by acoustic stimuli was similar to that evoked by the electrical cortical stimulation (9.19 +/- 5.55 mV versus 9.22 +/- 5.16 mV). There was a significant correlation between the parameters of the EPSPs evoked by an acoustic stimulus and those evoked by cortical stimulation. The mean amplitude of the IPSP evoked by electrical cortical stimulation was significantly greater than that evoked by acoustic stimuli (11.6 +/- 3.8 mV versus 9.1 +/- 3.7 ms, P < 0.05). Seven auditory EPSP and 7 IPSP neurones were examined with corticofugal modulation and labelled with Neurobiotin. Of the 7 EPSP neurones, 5 showed excitatory responses to cortical stimulation and 2 demonstrated no effects. Four of the 5 neurones that received corticofugal depolarization were located in the lemniscal MGB and 1 in the non-lemniscal MGB; of the remaining 2, 1 was located in the lemniscal and the other in the non-lemniscal MGB. Of the 7 IPSP neurones, 1 received an excitatory corticofugal input followed by an inhibitory input and 4 received only an inhibitory corticofugal input, while the remainder demonstrated no corticofugal effects. All 7 neurones were located in the non-lemniscal MGB. The result that both ascending and descending inputs caused similarly shaped EPSPs reflects a neuronal endogenous characteristic irrespective of the physical locations of the synapses. The IPSP responses to both acoustic stimuli and electrical cortical stimulation are likely to be caused by feedback from the thalamic reticular nucleus.

Figure 1. Electrical cortical stimulation potentiates the membrane potential of three MGB neurones that showed EPSPs to acoustic stimuli

The left and right panels show auditory responses without and with cortical stimulation, respectively. The neurone in A had a resting membrane potential of −57 mV, and that in B, −60 mV. The neurone in A was examined with 1 electrical pulse and 20 electrical pulses in the auditory cortex. The stimulation current was 100 μA.

Figure 2. An MGB neurone received corticofugal depolarization in its membrane potential

A, the MGB neurone responded to an acoustic stimulus with a spike and EPSP. B, the membrane potential was depolarized by cortical stimulation. Scale bars apply to both A and B. C, the neurone showed a frequency preference. Five trials of responses to pure-tone stimuli at 60 dB sound pressure level are shown at each of the following frequencies: 1, 4, 6 and 14 kHz.

Figure 3. Neuronal responses to acoustic stimulus and cortical stimulation

The left panel shows neuronal responses to a noise-burst stimulus of three MGB neurones (A, B and C) and the right panel shows the neuronal responses of corresponding neurones to a cortical stimulation followed by a noise-burst stimulus. Scale bars apply to all traces.

Figure 4. Mean amplitudes, rise times, decay times and durations of the postsynaptic potentials of the MGB neurones evoked by an auditory stimulus and by cortical stimulation

A, the means of the EPSPs evoked by the auditory stimuli (A Evoked, open columns) and by electrical cortical stimulation (E-Cx Evoked, grey columns). B, the means of the A-Evoked and E-Cx-Evoked IPSPs. Comparisons were made between the means of the A-Evoked and E-Cx-Evoked IPSPs using Student's paired t test. *P < 0.05; **P < 0.01.

Figure 5. The anatomical locations of the MGB neurones showed varied response patterns to electrical cortical stimulation

The neurones in A–C showed EPSP responses to the acoustic stimulus and EPSP responses to electrical cortical stimulation. The neurones in (D–F) showed inhibitory responses to electrical cortical stimulation. The left panels show physiological responses to acoustic stimuli and to electrical stimulation; the centre panels show the morphologies of the recorded neurones that were labelled with Neurobiotin; the right panels show lower magnifications for the sections after they were counterstained with neutral red. Recorded neurones injected with Neurobiotin were labelled in dark brown after the DAB reaction, as shown in the centre panels. The neurones in the middle panels of (A–C and E) were photographed before they were further processed with neutral red staining, as shown in the right panels. The subdivisions of the MGB were parcelled based on the neural architectures of neutral red staining. v, Ventral nucleus; s, shell nucleus; cm, caudomedial nucleus; rm, rostromedial nucleus of the MGB. Scale bars: centre panels, 100 μm; right panels, 1000 μm.

Figure 6. Response of the membrane potential to an auditory stimulus, spontaneous spike, and cortical stimulation of an MGB neurone

A, the neurone responded to repeated noise-burst stimuli with IPSPs. B, changes in the membrane potential after a spontaneous spike. C, reponses to cortical stimulations. The scale bars of the membrane potential and time apply to all traces.

Figure 7. Responses of the membrane potential to auditory stimuli, spontaneous spikes and cortical stimulations of an MGB neurone

A, the neurone responded to a noise-burst stimulus with two spikes and an IPSP. B, change in the membrane potential after spontaneous spike trains. The inset shows the indicated area at a higher magnification. C, response to cortical stimulation. D, responses to auditory stimuli in various postspontaneous periods. The scale bars of membrane potential and time apply to all traces except that in the inset of B.

Figure 8. Anatomical location and responses of membrane potential to acoustic stimuli and cortical stimulations of an MGB neurone

A, responses to repeated acoustic stimuli. B and C, responses to electrical stimulations of one and four pulses. Scale bars in C apply to A–C. D, anatomical location of the recorded neurone. The neurone was labelled with Neurobiotin and counterstained with neutral red. The inset at the top right shows the indicated area at a higher magnification. Scale bar, 1000 μm.

Figure 9. Neuronal responses to a combination of electrical stimulation and an auditory stimulus

The resting membrane potential was −62 mV and the scale bars apply to both traces.