Intracellular recordings in response to monaural and binaural stimulation of neurons in the inferior colliculus of the cat

Abstract

The inferior colliculus (IC) is a major auditory structure that integrates synaptic inputs from ascending, descending, and intrinsic sources. Intracellular recording in situ allows direct examination of synaptic inputs to the IC in response to acoustic stimulation. Using this technique and monaural or binaural stimulation, responses in the IC that reflect input from a lower center can be distinguished from responses that reflect synaptic integration within the IC. Our results indicate that many IC neurons receive synaptic inputs from multiple sources. Few, if any, IC neurons acted as simple relay cells. Responses often displayed complex interactions between excitatory and inhibitory sources, such that different synaptic mechanisms could underlie similar response patterns. Thus, it may be an oversimplification to classify the responses of IC neurons as simply excitatory or inhibitory, as is done in many studies. In addition, inhibition and intrinsic membrane properties appeared to play key roles in creating de novo temporal response patterns in the IC.

Fig. 15.

An ITD-sensitive neuron recorded extracellularly in the IC of an unanesthetized rabbit that displayed response properties consistent with the intracellular records in Figure 14.A, Poststimulus time histogram (PSTH) to contralateral (contra) tone bursts (70 dB SPL, 50 repetitions).B, PSTH to ipsilateral (ipsi) tone bursts (same parameters as in A, but 20 repetitions).C, PSTH to a 1 Hz binaural-beat stimulus (contra, 600 Hz; ipsi, 601 Hz; both 70 dB SPL; 4 repetitions).

Fig. 1.

Examples of responses to contralateral stimulation from nine IC neurons (A–I). In each case, the responses to the initial presentation of a 50 msec tone burst at or near the best frequency of the neuron are shown. Horizontal bars in this and subsequent figures represent the stimulus duration. Frequency and intensity of the tone bursts are indicated.

Fig. 9.

A neuron that showed inhibition to ipsilateral stimulation, complex excitation, and inhibition to contralateral stimulation, and yet the binaural response resembled that to contralateral stimulation. In all records, the responses to six identical tone bursts (65 dB SPL) were averaged at each of the frequencies indicated. A–D (first column), Responses to stimulation of the ipsilateral (IPSI) ear. In all cases, ipsilateral tone bursts evoked a short-latency hyperpolarization that slowly decayed over the stimulus duration. E–H (second column), Responses to stimulation of the contralateral (CONTRA) ear. Tone bursts evoked a transient depolarization, followed by a transient hyperpolarization, which was then followed by a sustained depolarization that lasted throughout the stimulus duration.I–L (third column), Predicted binaural response was estimated by summing the ipsilateral (first column) and contralateral (second column) responses.M–P (fourth column), Actual responses to binaural stimulation (same stimulus parameters as in thefirst and second columns). Responses are from the same neuron as in Figures 5 (right column) and 7.

Fig. 13.

An ITD-sensitive neuron that had an inhibitory–excitatory response to contralateral stimulation and an excitatory–inhibitory response to ipsilateral stimulation.A, Response to three sequential contralateral (Contra) tone bursts (80 dB SPL). B, Response to three sequential ipsilateral (Ipsi) tone bursts (80 dB SPL). C, Response to a 3 Hz binaural-beat stimulus (contra, 2100 Hz; ipsi, 2103 Hz; both at 80 dB SPL). The sinusoid (bottom) is at the beat frequency. The discharge follows the beat frequency, and this is seen more clearly in Figure 11C, where the response to the binaural-beat stimulus is plotted as a function of ITD.

Fig. 14.

An ITD-sensitive neuron that had a predominant inhibitory response to contralateral, ipsilateral, and binaural stimulation. A, Averaged response (35 repetitions) to contralateral (contra) tone bursts (65 dB SPL).B, Averaged response (10 repetitions) to ipsilateral (ipsi) tone bursts (same stimulus parameters as inA). C, Averaged response (3 repetitions) to a 3 Hz binaural-beat stimulus (contra, 1000 Hz;ipsi, 1003 Hz; both at 65 dB SPL). The horizontal dotted line indicates the resting potential.

Fig. 2.

Examples of responses to ipsilateral stimulation from four IC neurons (A–D). Same format as Figure 1. The inhibition in A was more clearly evident when the response to 15 stimulus repetitions was averaged (not shown).

Fig. 6.

A neuron that showed binaural suppression occurring within the IC. Shown are the responses to the first two tone bursts at the frequencies and levels indicated. Action potentials have been cropped. A, D, G (left column), Responses to ipsilateral (IPSI) tone bursts. A transient hyperpolarization (arrows) near stimulus onset was seen in all records. B, E, H (middle column), Responses to contralateral (CONTRA) tone bursts, which evoked a sustained depolarization and action potentials that were tightly coupled to the stimulus onset. C, F, I(right column), Responses to binaural stimulation.. Binaural responses were attenuated relative to contralateral responses both in the number of action potentials and level of sustained depolarization. The best excitatory response of the neuron was near 3500 Hz. Same neuron as in Figures 1G and 3 (right column).

Fig. 3.

Two neurons that displayed inhibitory side bands.A–F (left column), Responses of one neuron to tone bursts from 500 to 5000 Hz. Each panel is the response to two successive tone bursts (80 dB SPL) at the frequencies indicated. The best frequency was 3500 Hz (D).Arrows mark the transient hyperpolarizations seen at the edges of the response area of this neuron (A, F). Action potentials have been cropped. Responses are from the neuron of Figure 1G. G–L (right column), Responses of another neuron to tone bursts from 5 to 11 kHz. Here, the responses to six identical tone bursts (65 dB SPL) were averaged at each of the frequency indicated. Best frequency is near 9 kHz (J).

Fig. 8.

A binaural neuron that showed a long-latency excitation to stimulation of either ear. A, Ipsilateral (IPSI) responses to two sequential tone bursts (1.5 kHz) reveals a late depolarization accompanied by a spike or two.B, Same stimulus as in A delivered to the contralateral (CONTRA) ear evoked a similar response.C–F (right column), Responses to binaural stimulation at the contralateral and ipsilateral levels indicated. Binaural responses systematically declined as the level to the ipsilateral ear was reduced until the response resembled the response to contralateral stimulation (F). Binaural responses were not tested at the same levels as the monaural responses.

Fig. 4.

A third example of a neuron that displayed inhibitory side bands. The responses of the cell to a single tone burst (50 dB SPL) at the frequencies indicated are shown. Dotted lines indicate the resting potential of the neuron. Driven action potentials occurred near stimulus onset (arrows). Spontaneous activity was ∼31 spikes/sec. A, Lower-frequency inhibitory side band (14 kHz); B, best frequency of the neuron (17 kHz); C, upper-frequency inhibitory side band (20 kHz).

Fig. 5.

A neuron that displayed inhibitory side bands and synchronized to the envelope of sinusoidally amplitude-modulated tones only in the excitatory region. A–D, Left column, Averaged responses (n = 6) to a 3 Hz binaural-envelope beat stimulus (contralateral modulation, 100 Hz; ipsilateral modulation, 103 Hz) at the carrier frequencies indicated.Horizontal dotted lines indicate the resting potential. Synchronized oscillations that followed the contralateral modulation frequency were present at excitatory frequencies (B, C) but little, if any, synchrony at inhibitory carrier frequencies (A, D). A–D, Right column, Frequency content of each response obtained by Fourier analysis. Amplitudes are peak to peak. A peak at the contralateral modulation frequency (100 Hz) was present only at excitatory frequencies. Same neuron as in Figure 3(right column).

Fig. 7.

A binaural neuron that displayed a transient excitation to contralateral stimulation but did not respond to ipsilateral stimulation. Illustrated are the records to two sequential tone bursts (11 kHz) at the intensities indicated. A, Ipsilateral (IPSI) stimulation did not evoke a response. B, D, G (middle column), Contralateral (CONTRA). Each tone burst evoked a transient depolarization and two closely spaced action potentials that were tightly coupled to stimulus onset. C, E, H(right column), Binaural responses were attenuated relative to contralateral responses both in the number of action potentials and level of the transient depolarization. F, Contralateral response when resting potential was large relative to the other records displayed. Response profiles to identical stimuli (F, G) were similar despite differences in the magnitude of the resting and action potentials.

Fig. 10.

An ITD-sensitive neuron that responded with excitation to stimulation of either ear. A, Response to three sequential contralateral (Contra) tone bursts (40 dB SPL). B, Response to ipsilateral (Ipsi) stimulation using same stimulus parameters as inA. C, response to a 3 Hz binaural-beat stimulus (contra, 450 Hz; ipsi, 453 Hz; both at 40 dB SPL).

Fig. 11.

Interaural delay curves generated from the response to the binaural-beat stimulus (for details, see Yin and Kuwada, 1983; Kuwada et al., 1987). A–D, From neurons in Figures 10, 12, 13, and 14, respectively. A–Creflect spike rates, whereas D was derived from the synaptic potentials synchronized to the beat frequency in Figure 14. Response in C represents average spike rates to 25 cycles of the binaural-beat frequency. Open andfilled squares denote spike rates (spikes per second) to contralateral (contra) and ipsilateral (ipsi) stimulation, respectively.

Fig. 12.

An ITD-sensitive neuron that displayed a pauser response pattern to contralateral stimulation at 60–90 dB SPL. The response to ipsilateral stimulation was not tested. A, Responses to contralateral (Contra) tone bursts at the stimulus levels indicated. B, Response to a 3 Hz binaural-beat stimulus (contra, 600 Hz;ipsi, 603 Hz; both at 80 dB SPL).

Fig. 16.

Iontophoretic injection of HRP after completing the recordings in Figure 13 resulted in two impregnated neurons that abutted each other and had similar morphological features.A, Sagittal view indicated a medium-sized neuron with spine-covered dendrites. B, sagittal view of the second cell had features similar to those of the neuron in A.C, coronal view of the neuron in A. Dendrites were highly oriented. D, coronal view of the neuron in B. Dendrites were highly oriented and lay in the same plane as C. D, Sagittal section through the lateral part of the IC indicates the position of the 2 cells. D–V, Dorsal–ventral plane; C–R, caudal–rostral plane.