Induced cortical responses require developmental sensory experience

Abstract

Sensory areas of the cerebral cortex integrate the sensory inputs with the ongoing activity. We studied how complete absence of auditory experience affects this process in a higher mammal model of complete sensory deprivation, the congenitally deaf cat. Cortical responses were elicited by intracochlear electric stimulation using cochlear implants in adult hearing controls and deaf cats. Additionally, in hearing controls, acoustic stimuli were used to assess the effect of stimulus mode (electric versus acoustic) on the cortical responses. We evaluated time-frequency representations of local field potential recorded simultaneously in the primary auditory cortex and a higher-order area, the posterior auditory field, known to be differentially involved in cross-modal (visual) reorganization in deaf cats. The results showed the appearance of evoked (phase-locked) responses at early latencies (<100 ms post-stimulus) and more abundant induced (non-phase-locked) responses at later latencies (>150 ms post-stimulus). In deaf cats, substantially reduced induced responses were observed in overall power as well as duration in both investigated fields. Additionally, a reduction of ongoing alpha band activity was found in the posterior auditory field (but not in primary auditory cortex) of deaf cats. The present study demonstrates that induced activity requires developmental experience and suggests that higher-order areas involved in the cross-modal reorganization show more auditory deficits than primary areas.

Keywords: cochlear implant; congenital deafness; cortical oscillations; secondary field; sensory deprivation.

Figure 1

Recording positions in the posterior auditory field. (A) Photograph of the cortex after trephination revealing the sulcal patterns in the cat. (B) Schematic illustration of the penetrations in PAF in their relative position to the posterior ectosylvian sulcus. With two recording depths, each penetration includes 32 recording sites in total. A dense mapping of the field allowed capturing the auditory responses in each animal. (C) Reconstruction of a microelectrode penetration stained with a fluorescence dye from a histological section in a deaf cat. The DiI-stained images were stacked and aligned to reconstruct the penetration. (D) Nissl staining from the same section as in C demonstrates recordings in supragranular layers. AES = anterior ectosylvian sulcus; C = caudal; D = dorsal; L = lateral; M = medial; PES = posterior ectosylvian sulcus; R = rostral; SSS = suprasylvian sulcus; V = ventral.

Figure 2

Examples of local field potentials and unit responses. (A) Unipolar LFP examples for electrically-stimulated hearing controls (blue) and deaf animals (red) in field A1 and the higher-order field PAF. Individual trials and their average are shown in colour and black, respectively, with P_a, N_b, P₁ components. (B) Same as A for bipolar derivation (b-LFP) response—eliminating the influence of the common reference and minimizing volume conduction. (C) Same as A for individual multiunit responses plotted as peristimulus time histograms (PSTHs). (D) The statistical distribution of peak-latencies for unipolar LFPs. (E) Same as D for b-LFPs. (F) Same as D for multi-unit activity peak-latencies. All responses were elicited by intracochlear electrical stimulation at the intensity of 6 dB above the site-threshold. D–F show significantly longer peak latencies in PAF than in A1 (P < 0.001), two-tailed Wilcoxon rank-sum test. *P < 0.05; ***P < 0.001; n.s. = not significant.

Figure 3

Time-frequency representation of the responses in an electrically-stimulated hearing control. TFRs of total (left, A and D), evoked (middle, B and E), and induced (right, C and F) responses in the primary A1 (upper, A–C) and the higher-order PAF (lower, D–F) from b-LFP signals in response to electric stimulation in a hearing control at the intensity of 6 dB above the site-threshold. Data are shown in decibel relative to the baseline (−400 ms to −100 ms prestimulus). Phase-locked evoked responses appear mainly at early latencies (<100 ms) while the non-phase-locked induced responses appear dominantly at late latencies (>100 ms).

Figure 4

Grand mean and statistical comparison of evoked and induced TFR. (A–H) Grand mean of evoked (A, B, E and F), and induced (C, D, G and H) TFR responses from b-LFP in hearing electrically-stimulated controls (A–D), and CDCs (E–H) in field A1 and PAF. The evoked activity appeared at early-latency (<100 ms), while the late-latency responses (>100 ms) represent induced activity. All TFRs are shown in decibel relative to baseline (−400 ms to −100 ms prestimulus). (I–L) Results of non-parametric cluster-based permutation statistical testing (cluster α threshold 1%, two-tail significant α-value = 0.5%) for comparison between hearing and deaf animals. Data are shown in t-values, significant regions are outlined by black lines. (I) A1 evoked response comparison (A and E). (J) PAF evoked response comparison (B and F). (K) A1 induced response comparison (C and G). (L) PAF induced response comparison (D and H).

Figure 5

Grand mean and statistical comparison of evoked and induced TFR for acoustic stimulation. (A–D) Grand mean of evoked (A and B), and induced (C and D) TFR responses from b-LFP of acoustic-stimulated hearing controls in field A1 and PAF. All TFRs are shown in decibel relative to the baseline (−400 ms to −100 ms prestimulus). (E–H) Results of non-parametric cluster-based permutation statistical testing (cluster α threshold 1%, two-tail significant α-value = 0.5%) for the acoustic-stimulated and electrically-stimulated hearing groups comparison. (E) Evoked response comparison in A1 (A and Fig. 4A). (F) Evoked response comparison in PAF (B and Fig. 4B). (G) Induced response comparison in A1 (C and Fig. 4C). (H) Induced response comparison in PAF (D and Fig. 4D). Here, the induced late-latency activities in PAF were significantly stronger than in the hearing, acutely deafened animals.

Figure 6

Power spectra of ongoing activity. (A) Grand median power spectra comparison of ongoing activity in hearing animals with intact cochlea (IC, green), hearing acutely deafened animals (AD, blue), and congenitally deaf animals (CD, red) for A1 (shaded areas representing the upper and lower quartiles). Statistical pair comparisons are shown for hearing versus deaf (magenta line above the graph) and animals with intact cochleae versus acutely deafened cochleae (cyan line above the graph) using two-tailed Wilcoxon rank-sum test (FDR corrected q < 0.001). Hearing animals with intact cochlea show significantly more power in the baseline throughout all frequencies than all other groups. (B) Same as (A) for PAF. (C) Relative difference in the power of ongoing activity between hearing acutely deafened and deaf animals, showing stronger alpha power (10 Hz peak) in hearing animals. Black line = A1; grey line = PAF. (D) Same as C between hearing animals with intact cochlea and those after acute deafening. More ongoing power was found in animals with intact cochleae throughout all frequencies, whereas in A1 it was most prominent in alpha and beta range. Black line = A1; grey line = PAF.