High Spectral and Temporal Acuity in Primary Auditory Cortex of Awake Cats

Abstract

Most accounts of single- and multi-unit responses in auditory cortex under anesthetized conditions have emphasized V-shaped frequency tuning curves and low-pass sensitivity to rates of repeated sounds. In contrast, single-unit recordings in awake marmosets also show I-shaped and O-shaped response areas having restricted tuning to frequency and (for O units) sound level. That preparation also demonstrates synchrony to moderate click rates and representation of higher click rates by spike rates of non-synchronized tonic responses, neither of which are commonly seen in anesthetized conditions. The spectral and temporal representation observed in the marmoset might reflect special adaptations of that species, might be due to single- rather than multi-unit recording, or might indicate characteristics of awake-versus-anesthetized recording conditions. We studied spectral and temporal representation in the primary auditory cortex of alert cats. We observed V-, I-, and O-shaped response areas like those demonstrated in awake marmosets. Neurons could synchronize to click trains at rates about an octave higher than is usually seen with anesthesia. Representations of click rates by rates of non-synchronized tonic responses exhibited dynamic ranges that covered the entire range of tested click rates. The observation of these spectral and temporal representations in cats demonstrates that they are not unique to primates and, indeed, might be widespread among mammalian species. Moreover, we observed no significant difference in stimulus representation between single- and multi-unit recordings. It appears that the principal factor that has hindered observations of high spectral and temporal acuity in the auditory cortex has been the use of general anesthesia.

Keywords: Auditory cortex; Auditory filters; Frequency response area; Non-monotonic; Non-synchronized; Phase locking; Temporal representation; Tuning curve.

Fig. 1

Frequency response areas (FRAs) of three units recorded in one animal. In each panel, sound levels are shown on the vertical axis, tone frequencies are shown on the horizontal axis, and mean spike rates as percentages of the maximum rate for each unit are represented by colors. (a) V-shaped FRA from a well-isolated single unit. The BF and best level were 7.8 kHz and 35 dB SPL. (b) I-shaped FRA from a multi-unit recording. The BF and best level were 6.5 kHz and − 5 dB SPL. (c) O-shaped FRA from a multi-unit recording. The BF and best level were 6.1 kHz and − 20 dB SPL

Fig. 2

(a) Relationship between bandwidth at best level (vertical axis) and best frequency (horizontal axis). Dashed vertical lines indicate the range of best frequencies within ± 1 oct of 8 kHz. O and V/I units are distinguished by symbol shapes and colors, as indicated. (b) Bandwidth at best level versus best level. Values are jittered in the horizontal (best level) dimension to improve visibility

Fig. 3

Relationship between monotonicity index (vertical axis) and bandwidth at best level (horizontal axis). There was a significant correlation between monotonicity index and bandwidth at best level (r = 0.48, P < 10⁻⁶)

Fig. 4

Distribution of sustained indices (as defined in Results). Numbers of V/I and O units are distinguished by colors, as indicated

Fig. 5

(a) Post-stimulus-time histograms (PSTHs) for one unit. Each horizontal row of pixels represents a PSTH at a single frequency indicated on the vertical axis; in each row, responses are collapsed across sound levels from 40 to 90 dB SPL. Mean spike rates are represented by colors, with warmer colors denoting higher spike rates. The black bar at the bottom of the plot indicates the tone duration. (b, c, d) FRAs of the same unit computed for various time ranges re tone onset, as indicated in each panel. Colors indicate mean spike rates as percentages of the maximum rate for each time range. The color scale in panel d applies to panels b, c, and d

Fig. 6

Bandwidths of units exhibiting sustained responses computed for early (10–60 ms) and late (60–110) late times after tone onset. The analysis is limited to the units having non-zero sustained indices: N = 47 V/I units and N = 20 O units. Lines and bars denote medians and quartiles. The P values are from rank sum tests

Fig. 7

Temporal responses of a well-isolated single unit. (a) Each row of pixels represents a PSTH for a particular click rate indicated on the vertical axis. Mean spike rates are represented by colors, with warmer colors denoting higher spike rates. The black bar at the bottom of the panel indicates the duration of the click trains. (b) Each row of pixels represents a period histogram for a particular click rate. Each period histogram shows mean responses to clicks expressed as phase lags relative to the repetition period of the click train. The analysis was limited to the range of 100 to 1010 ms after the onset of the click train. (c) Summary measures plotted on a logarithmic scale of click rate. The blue solid line with triangles and the left vertical axis represent mean spike rates in the post-onset-range of 100 to 1010 ms as a function of click rate. Values are given as the mean spike rate minus the mean spontaneous rate for each unit. The red solid line with circles and the right vertical axis represent the vector strength, which is a measure of stimulus synchrony defined in the “Methods” section. The dashed red line indicates the criterion for significant phase locking. Vector strengths higher than the criterion (denoted by filled circles) were significant according to the Rayleigh test described in Methods (P < .001). (d) Cumulative phase lag, plotted on a linear scale of click rate. Data are plotted only for click rates at which phase locking was significant. The solid line plots the regression. The group delay of 38.4 ms was computed from the slope of the regression line

Fig. 8

Temporal response of a well-isolated single unit, in this case showing phase locking at high click rates. Format of the 4 panels is identical to that in Fig. 7

Fig. 9

Cumulative distribution of synchronized units. The curves trace the percentage of multi-unit sites (blue lines) or well-isolated single units (dashed black lines) that were synchronized at each click rate (given on the horizontal axis). The unit counts (N) values are the counts of units that responded in any way to the click trains

Fig. 10

Temporal response of one unit, in this case showing suppression and offset responses to high click rates. Format of the 4 panels is identical to that in Fig. 7. In addition, the dashed blue line with X signs in panel c indicates mean rates of the offset responses (minus the mean spontaneous rate) as a function of click rate; the offset rate was computed over 10 to 190 ms after offset of the click trains. The values of those mean rates are given on the left axis

Fig. 11

Summary measures of temporal responses of two units. Format of the 2 panels is identical to that in Fig. 7(c). a This unit showed synchronized responses to click rates of 7.1, 10, and 14.4 cps and non-synchronized monotonically-increasing rate responses to click rates > 40 cps. b This unit showed synchronized responses to most click rates up to 80 cps and non-monotonic rate response to click rates ≥ 57 cps. In this case, the spike rate peaked at 160 cps and declined at higher click rates

Fig. 12

(a) Distribution of dynamic ranges of non-synchronized rate responses. All spike rates were computed in the range of 110–1010 ms after the onset of the click trains. Blue and black fill indicate multi- and single-unit responses, respectively. (b) Distribution of the depths of modulation of spike rates by varying click rates. The modulation depth was given by the maximum minus the minimum spike rates within the dynamic range of click rates as a percentage of the maximum minus minimum spike rates across all click rates

Fig. 13

Dynamic ranges of single units. Each horizontal bar depicts the dynamic range of one unit, either a multi-unit site (blue bars) or a well-isolated single unit (dashed black bars)