doi: 10.1152/jn.00167.2009. Epub 2009 Jul 1.
Functional specialization of medial auditory belt cortex in the alert rhesus monkey
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- PMID:19571201
- PMCID: PMC2746772
- DOI: 10.1152/jn.00167.2009
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Functional specialization of medial auditory belt cortex in the alert rhesus monkey
Pawel Kusmierek et al. J Neurophysiol.2009 Sep.
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Abstract
Responses of neural units in two areas of the medial auditory belt (middle medial area [MM] and rostral medial area [RM]) were tested with tones, noise bursts, monkey calls (MC), and environmental sounds (ES) in microelectrode recordings from two alert rhesus monkeys. For comparison, recordings were also performed from two core areas (primary auditory area [A1] and rostral area [R]) of the auditory cortex. All four fields showed cochleotopic organization, with best (center) frequency [BF(c)] gradients running in opposite directions in A1 and MM than in R and RM. The medial belt was characterized by a stronger preference for band-pass noise than for pure tones found medially to the core areas. Response latencies were shorter for the two more posterior (middle) areas MM and A1 than for the two rostral areas R and RM, reaching values as low as 6 ms for high BF(c) in MM and A1, and strongly depended on BF(c). The medial belt areas exhibited a higher selectivity to all stimuli, in particular to noise bursts, than the core areas. An increased selectivity to tones and noise bursts was also found in the anterior fields; the opposite was true for highly temporally modulated ES. Analysis of the structure of neural responses revealed that neurons were driven by low-level acoustic features in all fields. Thus medial belt areas RM and MM have to be considered early stages of auditory cortical processing. The anteroposterior difference in temporal processing indices suggests that R and RM may belong to a different hierarchical level or a different computational network than A1 and MM.
Figures
Spectrograms of the natural stimuli used in the experiment.A: monkey calls (bark, coo1, coo2, coo3, girney, grunt, harmonic arch, pant threat, scream1, scream2).B: environmental sounds (middle row: cage [sound of monkey swinging], cage divider, cage lock open, monkey chair latch close, monkey chair latch open;bottom row: monkey pole latch, moving food container, vacuum pump, VCR and TV turning on, water running in sink). The frequency axis of the spectrograms has a logarithmic scale.
Determining the core/belt boundary.A: distribution of band-pass noise/pure tone (BPN/PT) ratio obtained from the neurons' sustained responses [BPN/PT(s)] in the recording area. Data smoothed with a 2-dimensional Gaussian kernel, σ = 1.5. Black line shows the core/medial belt boundary. Belt areas are located medially and are predominantly red/yellow; core areas are located laterally and are predominantly blue/green. Location of units whose responses are shown inC andD is marked with white letters.B: direction, strength, and significance of BPN/PT(s) gradients. Correlation coefficient of the ratio values with spatial locations of units projected onto an axis that was rotated 360° in 5° steps is shown as a black line. The gradient direction angle is the angle at which maximum correlation was found, the strength is the maximum r value, and theP value is determined by comparison with correlations obtained from scrambled data (shades of gray). Seemethods for details. The outer circle of the plot denotesr = 0.4.C: example response of a belt unit, showing sustained activity to BPN stimuli.D: example response of a core unit, showing no sustained activity to BPN stimuli. Vertical lines show stimulus start and end. Peristimulus time histograms (PSTHs) binned with 20 ms.
Best (center) frequency gradients and determination of the anteroposterior division of the recording area.A: average best (center) frequency at each recording location. Data from PT and BPN combined, “on” response only.B: smoothed data with the boundary between anterior and posterior areas shown in black; core/belt boundary is shown in gray. Core field designations: A1, primary auditory field; R, rostral field. Medial belt field designations: MM, middle medial belt; RM, rostral medial belt.
Direction and magnitude of cochleotopic gradients in fields A1 (blue), R (red), MM (green), and RM (orange).A–C: polar plots of correlation coefficient of the best (center) frequency with a rotated axis (seemethods for details) for “on” (A), “sustained” (B), and “off” (C) response. On each plot, 3 lines in the same color show data from PT, 1/3-octave BPN, and 1-octave BPN.D: angles of gradients for each field and stimulus. Within each stimulus column, the left-hand markers show data from monkey L; the right-hand markers show data from monkey S. Dark-filled squares, “on” response; light-filled circles, “sustained” response; open diamonds, “off” response. For detailedr,P, and angle values, see Table 1.
Neural response latencies.A: response latency distributions for each field and monkey. Boxes show the median and quartiles; whiskers show the range. For each field, data from monkey L are shown on theleft, from monkey S on theright.B: relationship between response latency and unit's best (center) frequency [BF(c)], established for the stimulus bandwidth that provided the latency estimate; seemethods . WN, white noise; PN, pink noise. Data from both monkeys pooled. Blue: field A1; red: field R; green: field MM; orange: field RM. Overlapping data points have been slightly scattered along the frequency axis to improve figure clarity. Correlation coefficients are provided in Table 2. Lowercase letters denote data points illustrated by raster plots inC. The gray dashed line shows the sum of cochlear travel time estimate (Anderson et al. 1971), one wave period, and a 5-ms constant delay; seediscussion for details.C: spike raster plots obtained with the stimuli used to estimate latency of 8 example units, 2 for each field. Latency value, stimulus, and monkey designation are provided for each raster plot. Only relevant part of the neural response is shown; note different timescales. Red vertical line shows stimulus onset; green dashed line shows latency. These raster plots are corrected for sound travel time and window discriminator delay (seemethods ).
Temporal structure of neural responses.A: spectrograms of example environmental sounds and monkey calls. Line plots along each spectrogram's frequency axes show tuning profiles [rate-(center)frequency curves] of example units, whose responses to these sounds are shown below inB. Solid line, “on” tuning profile; dotted line, “sustained” tuning profile; line color indicates the cortical field in which the unit was found and matches the color of the unit's PSTHs inB. Tuning profiles averaged across PTs and BPNs. Plots normalized to maximum peak firing rate (PFR) produced by the unit in respective (“on” or “sustained”) response.B: PSTHs and raster plots obtained from example units in response to stimuli shown above inA. Each row contains examples from one cortical field: A1, R, MM, or RM. Individual monkeys are identified with letters L and S. Vertical lines show stimulus start and end. PSTHs binned with 20 ms. The PSTH ordinate shows spike count normalized to maximum spike count found for all stimuli in the unit. Individual responses are referenced using (a)–(q) labels when described inresults .C: PSTHs and raster plots obtained from example units in response to tones, band-pass, and wide-band noise bursts. PT, pure tone; BPN13, 1/3-octave band-pass noise; BPN1, 1-octave band-pass noise; PN, pink noise; WN, white noise; target, behavioral target (4-tone “melody”; only 12 first sweeps out of 96 obtained are shown in the raster plot for the target). Numbers show stimulus (center) frequency of PT and BPN in kilohertz. Responses in gray rectangle come from the same unit.D: effect of stimulus class and cortical field on best discriminator window. Significant differences marked with “>” signs (main effects) or with lines joining bars (post hoc comparisons). A: anterior fields (R + RM); P: more posterior fields (A1 + MM); C: core (R + A1); B: medial belt (RM + MM).
Performance of the linear pattern discriminator for 5 stimulus classes: ES, environmental sounds; MC, monkey calls; BPN1, 1-octave noise bursts; BPN13, 1/3-octave noise bursts; PT, pure tones.A: effect of analysis window on the average performance (proportion correct) of the discriminator. Chance level is 0.111 for PT and BPN and 0.1 for MC and ES.B: distribution of the best window, i.e., the window at which the discriminator performed best for each stimulus.
Comparison of best frequency calculated from responses to monkey calls (BFMC) and environmental sounds (BFES) with best (center) frequency [BF(c)] obtained from “on” responses to PT and BPN bursts.Left column: monkey calls;right column: environmental sounds.A: correlation of BFMC/BFES with BF(c). Color scale represents number of units.B: correlation of BFMC/BFES with BF(c) shuffled among the units.C: distributions of differences between BFMC/BFES and BF(c) (solid line) and between BFMC/BFES and shuffled BF(c) (dashed line).P values calculated with the F-test.
References
- Anderson DJ, Rose JE, Hind JE, Brugge JF. Temporal position of discharges in single auditory nerve fibers within the cycle of a sine-wave stimulus: frequency and intensity effects. J Acoust Soc Am 49: 1131–1139, 1971. - PubMed
- Anderson LA, Malmierca MS, Wallace MN, Palmer AR. Evidence for a direct, short latency projection from the dorsal cochlear nucleus to the auditory thalamus in the guinea pig. Eur J Neurosci 24: 491–498, 2006. - PubMed
- Behar I, Cronholm JN, Loeb M. Auditory sensitivity of the rhesus monkey. J Comp Physiol Psychol 59: 426–428, 1965. - PubMed
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