Ripples in the Anterior Auditory Field and Inferior Colliculus of the Ferret
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1 Ripples in the Anterior Auditory Field and Inferior Colliculus of the Ferret Didier Depireux Nina Kowalski Shihab Shamma Tony Owens Huib Versnel Amitai Kohn University of Maryland College Park Supported in part by the Air Force Office of Scientific Research, the Office of Naval Research, the National Science Foundation Grant CD and the National Institutes of Health.
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3 Methods! Responses of single units in AI, anterior field (AAF), and Inferior Colliculus (IC) in the barbiturate-anaesthetized ferret were recorded with single tungsten electrodes. Data were collected from a total of 7, 5 and 11 (resp.) ferrets, each weighing between kg.! Surgery and Animal Preparation: The techniques involved in the surgery and preparation for recording are described in detail in Shamma et al. (1993). The ferrets were anesthetized with pentobarbital sodium ( mg/kg IP) and maintained in an areflexic state using a continuous IV infusion of pentobarbital (~ 5 mg/kg/hr) diluted with dextrose-electrolyte solution for metabolic stability. Data collection typically lasted 6-7 hours.! Recording Procedures: Single-unit action potentials were recorded using glassinsulated tungsten microelectrodes with 5 to 6 MΩ impedances. The recorded signals were led through amplifiers and filters. Depending on the paradigm, a stimulus was presented every few seconds, and raster plots with 1ms time resolution were produced.! In AI, recordings were typically made at depths of 3-6 µm (layers III and IV). In AAF, electrode penetrations were made parallel to the depth of the suprasylvian sulcus (SSS), approximately.5 mm caudal of the sulcus so that cortical layers III and/or IV were reached. IC was exposed by removal of (visual) cortex, and electrodes were lowered until ICC was reached, following standard criteria.
4 Change in Ripple Phase 2 1 Ω = 1. cyc/oct Tonotopic Axis Amplitude Phase (degrees) 36
5 2 1 Measuring the Ripple Transfer Function 1. cyc/oct. cyc/oct. cyc/oct Tonotopic Axis Phase.5 Amplitude Ripple Frequency (cyc/oct) 2
6 .8 cycles/octave at 8 different phases Stimulus onset: 1 ms Stimulus offset: 15 ms phase ripple at 6 different ripple freq.
7 Tuning as a function of Ripple Frequency and Phase Ripple phase (degrees) Amplitude Phase (radians) Ripple Frequency (cyc/oct)
8 Response fields of varying bandwidth Τ(Ω) Φ (Ω) RF A Spike 8 Ωo= φ (radians) 2π -2π -π -6π -8π φ o = Spike BF RF = 5.2 khz 157/1a B Spike Ωo= 2. φ (radians) 2π -2π -π -6π -8π φ o = - 11 Spike.5 BF RF = 5.9 khz 152/6d Ω (cycles/octave) -1π Ω (cycles/octave) Frequency (khz)
9 Response Fields with varying asymmetries Τ(Ω) Φ (Ω) RF A Spike B Spike Ω ο = Ω ο = Ω (cycles/octave) φ (radians) φ (radians) 2π -2π -π -6π -8π 2π -2π -π -6π -8π φ o = φ o = Ω (cycles/octave) Spike Spike BF RF = 9. khz BF RF = 7.6 khz Frequency (khz) 15/6e 157/3d
10 . The Anterior Cortical Field M SSS R H L L H H L H AAF AI Area of magnification AAF L AI
11 BF s and latencies are similar 2 N = 17 AAF 3 2 N = 168 AI BF(kHz) N = BF (khz) N = 165 AI 16 2 AAF Latency (ms) Latency (ms)
12 Bandwidths (BW2) are larger in AAF N = 128 AAF 2 N =151 AI BW2 (octaves) BW 2 (octaves) Bandwidth (Octaves) 6 2 AAF BF (khz) Bandwidth (Octaves) 6 2 AI BF (khz)
13 Tuning to Ripples tends to be lower in AAF 2 1 N = 9 AAF Ω = Best Stationary Ripple Frequency (cyc/oct) 6 2 N = 155 AI Ω (cyc/oct) Single Unit Cluster Ω (cyc/oct) RF s asymmetries are evenly distributed N = 5 AAF N = 155 AI Phi Phi
14 Predictions Using Stationary Ripples Response Field of Cell BF khz 16/6a Spectral Profile of stimulus khz BF Response of Cell to Profile Spike count 1 2 Measured Response Predicted Response Response to flat spectrum shift, δ (octaves)
15 The Inferior Colliculus Cer SC IC R L IC
16 . Of BF s and Latencies 2 1 N = 138 IC 3 2 N = 168 AI BF (khz) Single Unit Cluster BF (khz) 16 2 N = 1 IC 6 2 N = 165 AI Latency (ms) Latency (ms)
17 Bandwidths 3 2 N = 138 IC N = 151 AI BW 2 (octaves) BW 2 (octaves) 5 IC 5 Bandwidth (Octaves) BF (khz) Bandwidth (Octaves) BF (khz)
18 . Best Ripple Frequency 6 N = N=1 2 AI 6 2 IC Ω (cyc/oct) 2.8 Single Unit Cluster Ω (cyc/oct) 12 N = 53 8 Ω = Best Ripple Frequency Tuning at.2 (c/)/ Tuning at best ripple
19 RF s are more symmetrical in IC 3 2 N = 138 IC 2 N = 155 AI Phi Single Unit Cluster Phi
20 Temporal properties: Moving Ripples ω = Hz A t = ms t = 62.5 ms Tonotopic Axis Response Field of Cell t = 125 ms.5 16 Tonotopic Axis (khz) t = ms τ d τ m Expected Response Ω = ripple frequency in cycle/octaves ω = temporal frequency in Hz t
21 Responses to Moving Ripples Temporal Frequency (Hz) Ripple Frequency is. cycles/oct 175/12c Ω =. cyc/oct ω = to 32 Hz Time (ms) 3 sweeps per ω
22 . Step 1. From Spike to Period Histogram ω (Hz) Step 2. Magnitude and Phase of Best Fit Spike 2 T Ωο (ω) ω ο = best temporal frequency ω (Hz) 2 IR(t) Radians 8π 6π π 2π 2π Φ (ω) Ω ο Φ Ωο (ω) Φ Ωο () ω (Hz) F Time (ms) 18 2 Spike Time (sec) Impulse Response Function
23 .. Linearity of responses in the Auditory Cortex AI and AAF display similar characteristics Anterior Field: (A) Stimulus Spectrogram,S(x,t) (B)RF (x) (C) Σ RF (x) S(x,t) x (D) IR(t) (E) Predicted Response Frequency (khz) khz Time (sec) 181/21d Time (sec) * Time (sec) Time (sec)
24 . Predicting the Response to a Complex Stimulus Primary Auditory Cortex: (A) Stimulus Spectrogram,S(x,t) (B)RF (x) (C) Σ RF (x) S(x,t) x (D) IR(t) (E) Predicted Response +8 Hz at. cyc/ oct ρ = Hz at 1.2 cyc/ oct 17/3a Time (sec) Time (sec) ρ = Time (sec) Time (sec) 17/3a Time (sec) Time (sec) Time (sec) Predicted response Measured response
25 Inferior Colliculus Responses Temporal Frequency (Hz) 12 Ripple Frequency is.2 cyc/oct 2 189IC/2a Time (ms) IC/2a Ω =.2 cyc/oct ω = to 6 Hz Time (ms) 15 sweeps per ω
26 Summary! Stationary and traveling ripples can be used to extract spectral and temporal properties of auditory cortical neurons.! Linearity: Responses to a broad-band complex stimuli, decomposed into a linear combination of ripples, can be predicted by summing the neuronal responses to the individual ripples.! Only Cortical neurons are selective to ripple frequencies; Collicular neurons are low-pass with respect to ripple frequencies.! Therefore, AI and AAF neurons could perform a multi-scale analysis of spectral shape: the spectral profile is analyzed at different degrees of resolution by neurons with receptive fields of different best frequencies, bandwidths and asymmetries.
27 References! DeValois R. and DeValois K. (1988) Spatial Vision. New York: Oxford U. Press! Shamma S.A., Versnel H. and Kowalski N. (1995) Ripple analysis in ferret primary auditory cortex I. Response characteristics of single units to sinusoidally rippled spectra. Auditory Neuroscience 1(3), pp ! Shamma S.A. and Versnel H. (1995) Ripple analysis in ferret primary auditory cortex. II. Prediction of unit responses to arbitrary spectral profiles. Auditory Neuroscience 1(3), pp ! Versnel H., Kowalski N. and Shamma S.A. (1995) Ripple analysis in ferret primary auditory cortex.iii. Topographic distribution of ripple response parameters. Auditory Neuroscience 1(3), pp ! Schreiner C.E. and Calhoun B.M. (1995) Spectral envelope coding in cat primary auditory cortex: properties of ripple transfer functions. Auditory Neuroscience 1(1): 23 pages.! Kowalski N., Versnel H. and Shamma S.A. (1995) Comparison of responses in the anterior and primary auditory fields of the ferret cortex. J. Neurophys. 73(), pp ! Owens A. and Shamma S. Surface evoked potentials reveal selectivity to spectral shape features. ARO 96.! Kowalski N., D.A.D. and Shamma S.A. (1995) Analysis of dynamic spectra in ferret primary auditory cortex: I. Response characteristics of single units to moving rippled spectra.! Kowalski N., D.A.D. and Shamma S.A. (1995) Analysis of dynamic spectra in ferret primary auditory cortex: II. Prediction of unit responses to arbitrary dynamic spectra.
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