Neural Mechanisms Underlying Selectivity for the Rate and Direction of Frequency-Modulated Sweeps in the Auditory Cortex of the Pallid Bat

2006 ◽  
Vol 96 (3) ◽  
pp. 1303-1319 ◽  
Author(s):  
Khaleel A. Razak ◽  
Zoltan M. Fuzessery
Keyword(s):  
Auditory Cortex ◽  
High Frequency ◽  
Cortical Neurons ◽  
Arrival Time ◽  
Narrow Band ◽  
Low Frequency ◽  
Sweep Rate ◽  
Direction Selectivity ◽  
Pallid Bats ◽  
Pallid Bat

Frequency-modulated (FM) sweeps are common in vocalizations, including human speech. Selectivity for FM sweep rate and direction is present in the auditory cortex of many species. The present study sought to determine the mechanisms underlying FM sweep selectivity in the auditory cortex of pallid bats. In the pallid bat inferior colliculus (IC), two mechanisms underlie selectivity for FM sweep rate. The first mechanism depends on duration tuning for tones that arises as a consequence of early inhibition generated by an excitatory tone. The second mechanism depends on a narrow band of delayed high-frequency inhibition. Direction selectivity depends on a broad band of early low-frequency inhibition. Here, the contributions of these mechanisms to cortical FM sweep selectivity were determined in pentobarbital-anesthetized pallid bats. We show that the majority of cortical neurons tuned to echolocation frequencies are selective for the downward direction and rate of FM sweeps. Unlike in IC neurons tuned in the echolocation range, duration tuning is rare in cortical neurons with similar tuning. As in the IC, consistent spectrotemporal differences exist between low- and high-frequency sidebands. A narrow band of delayed high-frequency inhibition is necessary for FM rate selectivity. Low-frequency inhibition has a broad bandwidth, early arrival time, and creates direction selectivity. Cortical neurons respond better to slower FM rates and exhibit broader rate tuning than IC neurons. Relative arrival time of high-frequency inhibition is slower in the cortex than in the IC. Thus whereas similar mechanisms shape direction selectivity of neurons tuned in the echolocation range in the IC and the cortex, only one of the two mechanisms underlying rate selectivity in the IC is present in the cortex.

scholarly journals GABA Shapes Selectivity for the Rate and Direction of Frequency-Modulated Sweeps in the Auditory Cortex

2009 ◽  
Vol 102 (3) ◽  
pp. 1366-1378 ◽  
Author(s):  
Khaleel A. Razak ◽  
Zoltan M. Fuzessery
Keyword(s):  
Auditory Cortex ◽  
Gabaa Receptor ◽  
Gabaa Receptors ◽  
High Frequency ◽  
Arrival Time ◽  
Low Frequency ◽  
Direction Selectivity ◽  
Similar Response ◽  
Cortical Level ◽  
Pallid Bat

In the pallid bat auditory cortex and inferior colliculus (IC), the majority of neurons tuned in the echolocation range is selective for the direction and rate of frequency-modulated (FM) sweeps used in echolocation. Such selectivity is shaped mainly by spectrotemporal asymmetries in sideband inhibition. An early-arriving, low-frequency inhibition (LFI) shapes direction selectivity. A delayed, high-frequency inhibition (HFI) shapes rate selectivity for downward sweeps. Using iontophoretic blockade of GABAa receptors, we show that cortical FM sweep selectivity is at least partially shaped locally. GABAa receptor antagonists, bicuculline or gabazine, reduced or eliminated direction and rate selectivity in ∼50% of neurons. Intracortical GABA shapes FM sweep selectivity by either creating the underlying sideband inhibition or by advancing the arrival time of inhibition relative to excitation. Given that FM sweep selectivity and asymmetries in sideband inhibition are already present in the IC, these data suggest a refinement or recreation of similar response properties at the cortical level.

scholarly journals Differential roles of GABAergic and glycinergic input on FM selectivity in the inferior colliculus of the pallid bat

2011 ◽  
Vol 106 (5) ◽  
pp. 2523-2535 ◽  
Author(s):  
Anthony J. Williams ◽  
Zoltan M. Fuzessery
Keyword(s):  
Inferior Colliculus ◽  
Auditory System ◽  
High Frequency ◽  
Arrival Time ◽  
Drug Application ◽  
Low Frequency ◽  
Direction Selectivity ◽  
Central Nucleus ◽  
System 2 ◽  
Pallid Bat

Multiple mechanisms have been shown to shape frequency-modulated (FM) selectivity within the central nucleus of the inferior colliculus (IC) in the pallid bat. In this study we focus on the mechanisms associated with sideband inhibition. The relative arrival time of inhibition compared with excitation can be used to predict FM responses as measured with a two-tone inhibition paradigm. An early-arriving low-frequency inhibition (LFI) prevents responses to upward sweeps and thus shapes direction selectivity. A late-arriving high-frequency inhibition (HFI) suppresses slow FM sweeps and thus shapes rate selectivity for downward sweeps. Iontophoretic application of gabazine (GBZ) to block GABAA receptors or strychnine (Strych) to block glycine receptors was used to assess the effects of removal of inhibition on each form of FM selectivity. GBZ and Strych had a similar effect on FM direction selectivity, reducing selectivity in up to 86% of neurons when both drugs were coapplied. FM rate selectivity was more resistant to drug application with less than 38% of neurons affected. In addition, only Strych could eliminate FM rate selectivity, whereas GBZ alone was ineffective. The loss of FM selectivity was directly correlated to a loss of the respective inhibitory sideband that shapes that form of selectivity. The elimination of LFI correlated to a loss of FM direction selectivity, whereas elimination of HFI correlated to a loss of FM rate selectivity. Results indicate that 1) although the majority of FM direction selectivity is created within the IC, the majority of rate selectivity is inherited from lower levels of the auditory system, 2) a loss of LFI corresponds to a loss of FM direction selectivity and is created through either GABAergic or glycinergic input, and 3) a loss of HFI corresponds to a loss of FM rate selectivity and is created mainly through glycinergic input.

Functional Organization of the Pallid Bat Auditory Cortex: Emphasis on Binaural Organization

2002 ◽  
Vol 87 (1) ◽  
pp. 72-86 ◽  
Author(s):  
Khaleel A. Razak ◽  
Zoltan M. Fuzessery
Keyword(s):  
Auditory Cortex ◽  
Sound Localization ◽  
High Frequency ◽  
Functional Organization ◽  
Low Frequency ◽  
Frequency Region ◽  
Broadband Noise ◽  
Intensity Difference ◽  
Band Pass ◽  
Pallid Bat

This report maps the organization of the primary auditory cortex of the pallid bat in terms of frequency tuning, selectivity for behaviorally relevant sounds, and interaural intensity difference (IID) sensitivity. The pallid bat is unusual in that it localizes terrestrial prey by passively listening to prey-generated noise transients (1–20 kHz), while reserving high-frequency (<30 kHz) echolocation for obstacle avoidance. The functional organization of its auditory cortex reflects the need for specializations in echolocation and passive sound localization. Best frequencies were arranged tonotopically with a general increase in the caudolateral to rostromedial direction. Frequencies between 24 and 32 kHz were under-represented, resulting in hypertrophy of frequencies relevant for prey localization and echolocation. Most neurons (83%) tuned <30 kHz responded preferentially to broadband or band-pass noise over single tones. Most neurons (62%) tuned >30 kHz responded selectively or exclusively to the 60- to 30-kHz downward frequency-modulated (FM) sweep used for echolocation. Within the low-frequency region, neurons were placed in two groups that occurred in two separate clusters: those selective for low- or high-frequency band-pass noise and suppressed by broadband noise, and neurons that showed no preference for band-pass noise over broadband noise. Neurons were organized in homogeneous clusters with respect to their binaural response properties. The distribution of binaural properties differed in the noise- and FM sweep-preferring regions, suggesting task-dependent differences in binaural processing. The low-frequency region was dominated by a large cluster of binaurally inhibited neurons with a smaller cluster of neurons with mixed binaural interactions. The FM sweep-selective region was dominated by neurons with mixed binaural interactions or monaural neurons. Finally, this report describes a cortical substrate for systematic representation of a spatial cue, IIDs, in the low-frequency region. This substrate may underlie a population code for sound localization based on a systematic shift in the distribution of activity across the cortex with sound source location.

Mechanisms underlying intensity-dependent changes in cortical selectivity for frequency-modulated sweeps

2012 ◽  
Vol 107 (8) ◽  
pp. 2202-2211 ◽  
Author(s):  
K. A. Razak
Keyword(s):  
High Frequency ◽  
Cortical Neurons ◽  
Tuning Curve ◽  
Sound Intensity ◽  
Sweep Rate ◽  
Echolocation Calls ◽  
Wide Range ◽  
Species Specific ◽  
Neural Selectivity ◽  
Pallid Bat

Frequency-modulated (FM) sweeps are common components of species-specific vocalizations. The intensity of FM sweeps can cover a wide range in the natural environment, but whether intensity affects neural selectivity for FM sweeps is unclear. Bats, such as the pallid bat, which use FM sweeps for echolocation, are suited to address this issue, because the intensity of echoes will vary with target distance. In this study, FM sweep rate selectivity of pallid bat auditory cortex neurons was measured using downward sweeps at different intensities. Neurons became more selective for FM sweep rates present in the bat's echolocation calls as intensity increased. Increased selectivity resulted from stronger inhibition of responses to slower sweep rates. The timing and bandwidth of inhibition generated by frequencies on the high side of the excitatory tuning curve [sideband high-frequency inhibition (HFI)] shape rate selectivity in cortical neurons in the pallid bat. To determine whether intensity-dependent changes in FM rate selectivity were due to altered inhibition, the timing and bandwidth of HFI were quantified at multiple intensities using the two-tone inhibition paradigm. HFI arrived faster relative to excitation as sound intensity increased. The bandwidth of HFI also increased with intensity. The changes in HFI predicted intensity-dependent changes in FM rate selectivity. These data suggest that neural selectivity for a sweep parameter is not static but shifts with intensity due to changes in properties of sideband inhibition.

Auditory Imagery Modulates Frequency-specific Areas in the Human Auditory Cortex

2013 ◽  
Vol 25 (2) ◽  
pp. 175-187 ◽  
Author(s):  
Jihoon Oh ◽  
Jae Hyung Kwon ◽  
Po Song Yang ◽  
Jaeseung Jeong
Keyword(s):  
Auditory Cortex ◽  
High Frequency ◽  
Low Frequency ◽  
Primary Auditory Cortex ◽  
Auditory Imagery ◽  
Neural Responses ◽  
Top Down ◽  
Visual Areas ◽  
Control Functional ◽  
Response Area

Neural responses in early sensory areas are influenced by top–down processing. In the visual system, early visual areas have been shown to actively participate in top–down processing based on their topographical properties. Although it has been suggested that the auditory cortex is involved in top–down control, functional evidence of topographic modulation is still lacking. Here, we show that mental auditory imagery for familiar melodies induces significant activation in the frequency-responsive areas of the primary auditory cortex (PAC). This activation is related to the characteristics of the imagery: when subjects were asked to imagine high-frequency melodies, we observed increased activation in the high- versus low-frequency response area; when the subjects were asked to imagine low-frequency melodies, the opposite was observed. Furthermore, we found that A1 is more closely related to the observed frequency-related modulation than R in tonotopic subfields of the PAC. Our findings suggest that top–down processing in the auditory cortex relies on a mechanism similar to that used in the perception of external auditory stimuli, which is comparable to early visual systems.

Processing of frequency-modulated sounds in the cat's anterior auditory field

1994 ◽  
Vol 71 (5) ◽  
pp. 1959-1975 ◽  
Author(s):  
B. Tian ◽  
J. P. Rauschecker
Keyword(s):  
Pure Tone ◽  
Frequency Tuning ◽  
Broad Band ◽  
Low Frequency ◽  
Sweep Rate ◽  
Direction Selectivity ◽  
Neuron Activity ◽  
Complex Sounds ◽  
Range Rate ◽  
Auditory Field

1. Single-neuron activity was recorded from the anterior auditory field (AAF) in the cortex of gas-anesthetized cats. 2. Tone bursts and broad-band complex sounds were used for auditory stimulation. Responses to frequency-modulated (FM) sounds, in particular, were studied systematically. 3. Linear FM sweeps were centered around the best frequency (BF) of a neuron and had an excursion large enough to cover its whole frequency tuning range. Rate and direction of change of the FM sweeps were varied. 4. In 69% of the FM responses, a peak was found at an instantaneous frequency that corresponded to the BF in the pure-tone response. Thirty-three percent of the units had multiple maxima in their FM response. These secondary maxima were not always reflected in the pure-tone response of the same neurons. 5. The vast majority of AAF neurons showed one of two types of selectivity for FM rate. Depending on the criterion, almost half of the cells (46%) preferred fast changes of > 200 Hz/ms (high-pass) in both FM directions. Forty-eight percent of all neurons showed band-pass behavior with a clear preference in the middle range of FM rates in one or both directions. Low-pass or all-pass neurons made up only a small proportion (4 and 1%, respectively) of AAF neurons. 6. When both directions of an FM sweep (low-to-high and high-to-low-frequency) were tested, 66% of the neurons clearly were selective for one direction. This selectivity was not present necessarily at the preferred FM rate. In general, FM direction selectivity was most pronounced at slower FM rates. 7. The selectivity of AAF neurons for the rate and direction of FM sounds makes these neurons suitable for the detection and analysis of communication sounds, which often contain FM components with a particular sweep rate and direction.

scholarly journals Systems-based analysis of dendritic nonlinearities reveals temporal feature extraction in mouse L5 cortical neurons

2017 ◽  
Vol 117 (6) ◽  
pp. 2188-2208 ◽  
Author(s):  
Brian E. Kalmbach ◽  
Richard Gray ◽  
Daniel Johnston ◽  
Erik P. Cook
Keyword(s):  
High Frequency ◽  
Cortical Neurons ◽  
Action Potentials ◽  
Nonlinear Response ◽  
Functional Model ◽  
Low Frequency ◽  
Fast Variable ◽  
Nonlinear Component ◽  
Dendritic Spikes ◽  
Linear And Nonlinear

What do dendritic nonlinearities tell a neuron about signals injected into the dendrite? Linear and nonlinear dendritic components affect how time-varying inputs are transformed into action potentials (APs), but the relative contribution of each component is unclear. We developed a novel systems-identification approach to isolate the nonlinear response of layer 5 pyramidal neuron dendrites in mouse prefrontal cortex in response to dendritic current injections. We then quantified the nonlinear component and its effect on the soma, using functional models composed of linear filters and static nonlinearities. Both noise and waveform current injections revealed linear and nonlinear components in the dendritic response. The nonlinear component consisted of fast Na+ spikes that varied in amplitude 10-fold in a single neuron. A functional model reproduced the timing and amplitude of the dendritic spikes and revealed that they were selective to a preferred input dynamic (~4.5 ms rise time). The selectivity of the dendritic spikes became wider in the presence of additive noise, which was also predicted by the functional model. A second functional model revealed that the dendritic spikes were weakly boosted before being linearly integrated at the soma. For both our noise and waveform dendritic input, somatic APs were dependent on the somatic integration of the stimulus, followed a subset of large dendritic spikes, and were selective to the same input dynamics preferred by the dendrites. Our results suggest that the amplitude of fast dendritic spikes conveys information about high-frequency features in the dendritic input, which is then combined with low-frequency somatic integration. NEW & NOTEWORTHY The nonlinear response of layer 5 mouse pyramidal dendrites was isolated with a novel systems-based approach. In response to dendritic current injections, the nonlinear component contained mostly fast, variable-amplitude, Na+ spikes. A functional model accounted for the timing and amplitude of the dendritic spikes and revealed that dendritic spikes are selective to a preferred input dynamic, which was verified experimentally. Thus, fast dendritic nonlinearities behave as high-frequency feature detectors that influence somatic action potentials.

Disparity Modulation Sensitivity for Narrow-Band-Filtered Stereograms Viewed out of the Plane of Fixation

Perception ◽  
1996 ◽  
Vol 25 (1_suppl) ◽  
pp. 94-94
Author(s):  
B Lee ◽  
B J Rogers
Keyword(s):  
Spatial Frequency ◽  
High Frequency ◽  
Significant Interaction ◽  
Narrow Band ◽  
Low Frequency ◽  
Frequency Pattern ◽  
Spatial Frequencies ◽  
Size Disparity ◽  
Random Dot Stereograms

Narrow-band-filtered random-dot stereograms were used to determine stereo thresholds for detecting sinusoidal disparity modulations. These stereograms were designed to stimulate selectively channels tuned to luminance and corrugation spatial frequencies (Schumer and Ganz, 1979 Vision Research19 1303 – 1314). Thresholds were determined for corrugation frequencies ranging from 0.125 to 1 cycle deg−1, luminance centre spatial frequencies ranging from 1 to 8 cycles deg−1 and disparity pedestal sizes ranging from −32 to +32 min arc. For small disparity pedestals, lowest modulation thresholds were found around 0.5 cycle deg−1 corrugation frequency and 4 cycles deg−1 luminance centre spatial frequency. For large disparity pedestals (±32 arc min), lowest thresholds were shifted towards the lower corrugation frequencies (0.125 cycle deg−1) and lower luminance frequencies (2 cycles deg−1). There was a significant interaction between luminance spatial frequency and disparity pedestal size. For small pedestals, lowest thresholds were found with the highest luminance frequency pattern (4 cycles deg−1). For large pedestals, best performance shifted towards the low-frequency patterns (1 cycle deg−1). This effect demonstrates a massive reduction in stereo-efficiency for high-frequency patterns in the luminance domain at large disparity pedestals which is consistent with the ‘size-disparity relation’ proposed by previous researchers.

Processing of Frequency-Modulated Sounds in the Cat's Posterior Auditory Field

1998 ◽  
Vol 79 (5) ◽  
pp. 2629-2642 ◽  
Author(s):  
Biao Tian ◽  
Josef P. Rauschecker
Keyword(s):  
Frequency Tuning ◽  
Low Frequency ◽  
Sweep Rate ◽  
Direction Selectivity ◽  
Neuron Activity ◽  
Complex Sounds ◽  
The Difference ◽  
Range Rate ◽  
A Minor ◽  
Auditory Field

Tian, Biao and Josef P. Rauschecker. Processing of frequency-modulated sounds in the cat's posterior auditory field. J. Neurophysiol. 79: 2629–2642, 1998. Single-neuron activity was recorded from the posterior auditory field (PAF) in the cortex of gas-anesthetized cats. Tone bursts and broadband complex sounds were used for auditory stimulation. Responses to frequency-modulated (FM) sounds, in particular, were studied systematically. Linear FM sweeps were centered around the best frequency (BF) of a neuron and had an excursion large enough to cover its whole frequency tuning range. Rate and direction of change of the FM sweeps were varied. In the majority of PAF neurons (75%) the FM response seemed not to be linear, i.e., their best instantaneous frequency (BIF) varied by more than one octave at different FM rates (FMR). When the difference between BIF and BF at each FMR was used as a measure of linearity, it was within one-third octave only at five or fewer FMR in most PAF neurons (74%). The majority of PAF neurons (70%) preferred moderate FM rates (<200 Hz/ms). Fifty-four percent of all neurons in this area showed band-pass behavior with a clear preference in the middle range of FM rates in at least one direction. Overall, neurons with high-pass behavior in both directions made up only a minor portion (22%) of PAF neurons. When both directions of an FM sweep (low-to-high and high-to-low frequency) were tested, 50% of the neurons were clearly selective for one direction, i.e., the response to one FM direction was at least twice as large as that to the other direction. This selectivity was not necessarily present at the preferred FM rate. In general, FM direction selectivity was equally distributed over FM rates tested. The selectivity of PAF neurons for the rate and direction of FM sounds makes these neurons suitable for the detection and analysis of communication sounds, which often contain FM components with a moderate sweep rate in a particular direction.

Response selectivity for multiple dimensions of frequency sweeps in the pallid bat inferior colliculus

1994 ◽  
Vol 72 (3) ◽  
pp. 1061-1079 ◽  
Author(s):  
Z. M. Fuzessery
Keyword(s):  
Inferior Colliculus ◽  
High Frequency ◽  
Low Frequency ◽  
Central Nucleus ◽  
Frequency Change ◽  
Frequency Range ◽  
Low Frequencies ◽  
Response Properties ◽  
Sweep Direction ◽  
Pallid Bat

1. While hunting, the pallid bat uses passive sound localization at low frequencies to find terrestrial prey, and echolocation for general orientation. It must therefore process two different types of acoustic input at the same time. The pallid bat's echolocation pulse is a downward frequency-modulated (FM) sweep from 60 to 30 kHz. This study examined the response selectivity of single neurons in the pallid bat's central nucleus of the inferior colliculus (ICC) for FM sweeps, comparing the response properties of the high-frequency population, tuned to the biosonar pulse, with the low-frequency population, tuned below the pulse. The working hypothesis was that the high-frequency population would exhibit a response selectivity for downward FM sweeps that was not present in the low-frequency population. 2. Neurons were tested for their selectivity for FM sweep direction, duration, frequency range and bandwidth, and rate of frequency change. The extent to which they responded exclusively to tones, noise, and FM sweeps was also examined. Significant differences in the response properties of neurons in the two populations were found. In the low-frequency population, all neurons responded to tones, but only 50% responded to FM sweeps. Only 23% were selective for sweep direction. In the high-frequency population, all neurons responded to FM sweeps, but 31% did not respond to tones. Over one-half of this population was selective for sweep direction, and of those that were selective, all preferred the downward sweep direction of the biosonar pulse. A large percentage (31%) responded exclusively to downward sweeps, and not to tones or upward sweeps. None of the cells in either population responded to noise, or did so only at very high relative thresholds. 3. Both populations contained neurons that were selective for short stimulus durations that approximated the duration of the biosonar pulse, although the percentage was greater in the high-frequency population (58% vs. 20%). In the high-frequency population, 31% of the neurons tested for duration responded exclusively to both the sweep direction and duration of the biosonar pulse. 4. Downward FM-selective neurons, with one exception, were generally insensitive to the rate of frequency change of the FM sweep, as well as the frequency range and bandwidth of the sweep. They responded similarly to both the full 60- to 30-kHz sweep and to 5-kHz bandwidth portions of the full sweep.(ABSTRACT TRUNCATED AT 400 WORDS)

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