Plasticity of the cochleotopic (frequency) map in specialized and nonspecialized auditory cortices

Abstract

Auditory conditioning (associative learning) causes reorganization of the cochleotopic (frequency) maps of the primary auditory cortex (AI) and the inferior colliculus. Focal electric stimulation of the AI also evokes basically the same cortical and collicular reorganization as that caused by conditioning. Therefore, part of the neural mechanism for the plasticity of the central auditory system caused by conditioning can be explored by focal electric stimulation of the AI. The reorganization is due to shifts in best frequencies (BFs) together with shifts in frequency-tuning curves of single neurons. In the AI of the Mongolian gerbil (Meriones unguiculatus) and the posterior division of the AI of the mustached bat (Pteronotus parnellii), focal electric stimulation evokes BF shifts of cortical auditory neurons located within a 0.7-mm distance along the frequency axis. The amount and direction of BF shift differ depending on the relationship in BF between stimulated and recorded neurons, and between the gerbil and mustached bat. Comparison in BF shift between different mammalian species and between different cortical areas of a single species indicates that BF shift toward the BF of electrically stimulated cortical neurons (centripetal BF shift) is common in the AI, whereas BF shift away from the BF of electrically stimulated cortical neurons (centrifugal BF shift) is special. Therefore, we propose a hypothesis that reorganization, and accordingly organization, of cortical auditory areas caused by associative learning can be quite different between specialized and nonspecialized (ordinary) areas of the auditory cortex.

Figure 1

Cochleotopic (frequency) maps in the AIs of the Mongolian gerbil (A), mustached bat (B), and big brown bat (C). Iso-BF contour lines in the AI are shown by dashed lines. There are non-AI areas around the AI. The mean BFs of electrically stimulated cortical neurons are indicated by Xs. Almost all neurons studied in the gerbil and big brown bat were recorded from the shaded areas. In B, the DSCF area is a part of the AI. The areas anterior and posterior to the DSCF area are, respectively, called the AIa and AIp. The “FM–FM” area has an echo delay axis instead of a frequency axis. The frequency maps in A, B, and C are, respectively, based on Thomas et al. (7), Suga (24), and both Dear et al. (9) and Shen et al. (10). m.c.a., medial cerebral artery. The 0.5-mm scale applies for all three auditory cortices.

Figure 2

Changes in the frequency-response curves (a) and responses (b and c) of two cortical neurons (A and B) evoked by focal electric stimulation (ES_ar) of the AI of the gerbil. (a in A and B) Arrays of PSTC histograms displaying the responses to tone bursts at different frequencies. (b and c in A and B) PST histograms displaying the responses to the tone bursts at the BFs, in the control (BF_c, 3.50 kHz in A and 0.56 kHz in B) or shifted condition (BF_s, 2.75 kHz in A and 0.64 kHz in B. The 1, 2, and 3 show the responses in the control, shifted, and recovery conditions, respectively. The BF of the stimulated cortical neuron is indicated by the arrow in a2. The filled circles, X's, and open circles in a indicate the BFs in the control, shifted, and recovery conditions, respectively. The horizontal bars at the bottom of b and c represent 20-ms long tone bursts. The amplitude of tone bursts was fixed at 10 dB above minimum threshold of a given neuron.

Figure 3

Shifts in the BFs of 94 cortical neurons in the gerbil evoked by ES_ar as a function of difference in BF between recorded (AC_r) and stimulated cortical auditory neurons (AC_s). The BFs of AC_s ranged between 0.8 and 2.0 (1.25 ± 0.30) kHz. The data between −1.0 and +4.0 kHz BF differences in A are replotted on the expanded abscissa in B. The solid oblique lines are regression lines for data points (N) in given ranges of BF differences. a, slope; r, correlation coefficient. The horizontal dashed lines indicate one SD. The major BF shifts were centripetal, i.e., toward the BF of AC_s.

Figure 4

Changes in the frequency-response curves (a) and responses (b and c) of two cortical neurons (A and B) evoked by ES_ar of the posterior division of the primary auditory cortex (AIp) of the mustached bat. (a) Arrays of PSTC histograms displaying the responses to tone bursts at different frequencies. (b and c) PST histograms displaying the responses to the tone bursts at the BFs in the control (BF_c: 28.5 kHz in A and 52.5 kHz in B) or shifted condition (BF_s: 51.0 kHz in B), respectively. See Fig. 2 for symbols and other explanations.

Figure 5

Shifts in the BFs of 76 cortical neurons in the AIp of the mustached bat evoked by ES_ar as a function of difference in BF between AC_r and AC_s. The BFs of AC_s ranged between 6.8 and 54.0 (39.4 ± 4.3) kHz. The data between −4.0 and +4.0 kHz differences are replotted on the expanded abscissa in B. The major BF shifts were centripetal, i.e., toward the BF of AC_s. See Fig. 3 for abbreviations and other explanations.

Figure 6

Difference in BF shift among different mammalian species and between different cortical areas of a single species. BF shifts of cortical neurons along the frequency axis (ordinates) are plotted as a function of difference in BF (kHz) or distance (mm) between AC_r and AC_s. (A) AI of the Mongolian gerbil. (B) AI of the big brown bat (based on ref. 5). (C) AIp of the mustached bat. (D) DSCF area of the mustached bat (based on ref. 11). A pair of numbers in parentheses indicates a BF difference and BF shift in octave referring to the mean BF of AC_s. Focal electric stimulation of cortical auditory neurons evokes BF shifts of adjacent cortical neurons toward (centripetal shift; A, B, and C) or away from (centrifugal shift; D) the BF of AC_s. See the text.