Bilateral cortical interaction: modulation of delay-tuned neurons in the contralateral auditory cortex

Abstract

Transcallosal excitation and inhibition have been theorized based on the effect of callosotomy on intractable epilepsy and dichotic listening research, respectively. We studied bilateral interaction of cortical auditory neurons and found that this interaction consisted of focused facilitation and widespread lateral inhibition. The frequency modulated (FM)-FM area of the auditory cortex of the mustached bat is composed of delay-tuned neurons tuned to the combination of the emitted biosonar pulse and its echo with a specific echo delay [best delay (BD)] and consists of three subdivisions in terms of the combination sensitivity of neurons. We found that focal electric stimulation of one of these three subdivisions evoked BD shifts of delay-tuned neurons in all three subdivisions of the contralateral FM-FM area, presumably via the corpus callosum. The effect of electric stimulation of the delay-tuned neurons on the contralateral delay-tuned neurons was different depending on whether the BD of a recorded neuron was matched or unmatched in BD with that of the stimulated neurons. BD-matched neurons did not change their BDs and increased the responses at their BDs, whereas BD-unmatched neurons shifted their BDs away from the BD of the stimulated neurons and reduced their responses. The ipsilateral and contralateral BD shifts evoked by the electric stimulation were identical to each other. The contralateral modulation, in addition to the ipsilateral modulation, increases the contrast in the neural representation of the echo delay to which the stimulated neurons are tuned.

Figure 1.

Cortical auditory areas and the responses of a delay-tuned neuron. A, Dorsolateral view of the left cerebral cortex of the mustached bat. 1–6 are the DSCF, AIa (anterior division of the primary auditory cortex), Alp (posterior division of the AI), FM–FM, CF/CF, and DF (dorsal fringe) areas, respectively. B, The FM–FM area consists of three subdivisions in terms of combination sensitivity: FM₁-FM₂, FM₁-FM₃, and FM₁-FM₄. The subscripts 1–4 indicate the first through fourth harmonics of FM components of biosonar pulses and echoes. C, The array of PST histograms displaying the responses of a delay-tuned FM₁-FM₂ neuron to pulse FM₁ (P) alone, echo FM₂ (E) alone, and P-E pairs with different echo (E) delays ranging from 0 to 19 ms. The best delay for the facilitatory response of the neuron was 6 ms. An identical stimulus was delivered 50 times. FM₁, 28.5–22.5 kHz sweep at 40 dB SPL. FM₂, 58.0–46.0 kHz sweep at 20 dB SPL.

Figure 2.

BD shifts of an FM₁-FM₂ (A) and an FM₁-FM₄ (B) neuron evoked by electric stimulation of contralateral FM₁-FM₄ (A) or FM₁-FM₃ (B) neurons. Aa and Ba show delay–response curves obtained before (open circles; control), 60 min (A) or 50 min (B) after (filled circles), and 190 min (A) or 170 min (B) after (open triangle; recovery) the electric stimulation of the contralateral FM–FM neurons. P, Pulse FM₁; E, echo FM₂ (for A) and echo FM₄ (for B). The downward arrows indicate the BDs of the contralateral stimulated neurons. Each data point indicates a mean and SE. Ab, Ac, Bb, and Bc show PST histograms displaying the responses at the BDs of the given neurons in the control (BDc) and shifted (BDs) conditions. 1–3 show, respectively, the responses recorded before (control), 60 min (A) or 50 min (B) after, and 190 min (A) or 170 min (B) after (recovery) the electric stimulation. The dashed arrow in Aa indicates the delay width at 50% of the maximum response.

Figure 3.

The relationship between BD shifts and changes in 50% delay width. Each filled circle represents the datum obtained from a single neuron. r, Correlation coefficient.

Figure 4.

A, Distribution of BD shifts as a function of BD differences between the recorded FM–FM (Rec.) and electrically stimulated contralateral FM–FM neurons (cES). Open circles and triangles, Centrifugal (n = 29) and centripetal (n = 3) BD shifts measured in the normal bats, respectively. Filled circles, BD shifts (n = 17) measured in the bats with a lesioned collicular commissure. ×, No BD shifts (n = 7; 5 BD-unmatched neurons and 2 BD-matched neurons). The curve was obtained by averaging the data points at each BD difference and then two-point smoothing. B, The BD shifts of FM–FM neurons evoked by electric stimulation of ipsilateral (ipsi.; filled diamonds) and contralateral (contra.; open diamonds) FM–FM neurons. Each data point indicates a mean and SE. The numbers in the parentheses indicate the numbers of neurons from which the data were obtained. The data shown with the filled diamonds were obtained from the study by Xiao and Suga (2004).

Figure 5.

Changes in the response (A, B) and population (C) of FM–FM neurons evoked by electric stimulation of contralateral FM–FM neurons. A, Changes in the response magnitudes (mag.) of 53 FM–FM neurons at the BDs in the control (BDc; open circles) and shifted (BDs; filled circles) conditions evoked by electric stimulation of contralateral FM–FM neurons. Each data point indicates a mean and SE. B, Changes in the response magnitudes between the responses at the new (i.e., shifted) BD after electric stimulation and the original (i.e., control) BD before electric stimulation. The changes are expressed in percentage of the response of the control BD. C, Change in the population of FM–FM neurons tuned to different echo delays. The abscissa represents differences in BD between recorded (Rec.) and contralateral electrically stimulated (cES) FM–FM neurons.

Figure 6.

The mean time courses of the BD shifts (A) and changes in response magnitude (B) of 11 FM–FM neurons, which showed a 2 ms BD shift for electric stimulation of contralateral FM–FM neurons. Each symbol and a bar indicate a mean and SE, respectively. In B, the open and filled circles represent the changes in response magnitude at the control (original) and shifted (new) BDs, respectively.

Figure 7.

Frontal sections across the inferior colliculi. A, Normal brain. B, Brain with the 90% lesioned commissure of the inferior colliculus. Arrows indicate the commissure and electrolytic lesions. CBL, Cerebellum; IC, inferior colliculus; PAG, periaqueductal gray. Frozen sections of 50 μm are shown (cresyl violet stain).

Figure 8.

A BD shift evoked by focal electric stimulation of the contralateral FM–FM area in the bat with the ∼90% lesioned commissure of the inferior colliculus. a, Delay–response curves of an FM₁-FM₄ neuron obtained before (open circles; control), 50 min after (filled circles), and 150 min after (open triangles; recovery) the electric stimulation of contralateral FM₁-FM₂ neurons. P, Pulse FM₁; E, echo FM₄. The arrow indicates the BD of the stimulated contralateral neurons. Each data point indicates a mean and SE. b, c, PST histograms displaying the responses at the BDs of the FM₁-FM₄ neuron in the control (BD_c) and shifted (BD_s) conditions. 1–3 show, respectively, the responses recorded before (control), 50 min after, and 150 min after (recovery) the electric stimulation. CIC, Commissure of the inferior colliculus.