Cues for Sound Localization Are Encoded in Multiple Aspects of Spike Trains in the Inferior Colliculus

2008 ◽  
Vol 99 (4) ◽  
pp. 1672-1682 ◽  
Author(s):  
Steven M. Chase ◽  
Eric D. Young
Keyword(s):  
Inferior Colliculus ◽  
Discharge Rate ◽  
Spike Timing ◽  
Virtual Space ◽  
Dependent Manner ◽  
Single Neurons ◽  
Information Theoretic ◽  
Independent Information ◽  
Interaural Level Differences ◽  
Spike Latency

To localize sound, information from three cues—interaural timing differences (ITDs), interaural level differences (ILDs), and spectral notch cues (SNs)—must be properly integrated. The inferior colliculus (IC) receives convergent input from neurons encoding all three cues. Using virtual space stimuli and information theoretic techniques, we investigated the coding of the various localization cues in single neurons of the IC under different encoding schemes. Here we focus on the analysis of information encoded by first-spike latency, in comparison to previous results on discharge rate and ongoing spike timing. The results show that the localization cues converge to different degrees in particular neurons. ITD information is conveyed most strongly by spike rate, with small amounts of independent information in latency and ongoing spike timing. ILD information shows a similar pattern, with larger mutual information values for all three cues. For these cues, ongoing spike timing does not typically contribute independent information over that captured by a joint rate/first-spike latency code. SNs are coded by both rate and first-spike latency, but ongoing spike timing significantly enhances their representation in a best frequency–dependent manner, as long as the temporal envelope of the stimulus can be used in the decoder. The differential coding of the localization cues suggests that information about multiple cues could be multiplexed onto the responses of single neurons.

scholarly journals Information conveyed by inferior colliculus neurons about stimuli with aligned and misaligned sound localization cues

2011 ◽  
Vol 106 (2) ◽  
pp. 974-985 ◽  
Author(s):  
Sean J. Slee ◽  
Eric D. Young
Keyword(s):  
Inferior Colliculus ◽  
Sound Localization ◽  
Virtual Space ◽  
Central Nucleus ◽  
Single Neurons ◽  
Interaural Time Differences ◽  
Marmoset Monkey ◽  
Interaural Level Differences ◽  
Broadband Sound ◽  
Response Area

Previous studies have demonstrated that single neurons in the central nucleus of the inferior colliculus (ICC) are sensitive to multiple sound localization cues. We investigated the hypothesis that ICC neurons are specialized to encode multiple sound localization cues that are aligned in space (as would naturally occur from a single broadband sound source). Sound localization cues including interaural time differences (ITDs), interaural level differences (ILDs), and spectral shapes (SSs) were measured in a marmoset monkey. Virtual space methods were used to generate stimuli with aligned and misaligned combinations of cues while recording in the ICC of the same monkey. Mutual information (MI) between spike rates and stimuli for aligned versus misaligned cues were compared. Neurons with best frequencies (BFs) less than ∼11 kHz mostly encoded information about a single sound localization cue, ITD or ILD depending on frequency, consistent with the dominance of ear acoustics by either ITD or ILD at those frequencies. Most neurons with BFs >11 kHz encoded information about multiple sound localization cues, usually ILD and SS, and were sensitive to their alignment. In some neurons MI between stimuli and spike responses was greater for aligned cues, while in others it was greater for misaligned cues. If SS cues were shifted to lower frequencies in the virtual space stimuli, a similar result was found for neurons with BFs <11 kHz, showing that the cue interaction reflects the spectra of the stimuli and not a specialization for representing SS cues. In general the results show that ICC neurons are sensitive to multiple localization cues if they are simultaneously present in the frequency response area of the neuron. However, the representation is diffuse in that there is not a specialization in the ICC for encoding aligned sound localization cues.

Context Dependency in the Globus Pallidus Internal Segment During Targeted Arm Movements

2001 ◽  
Vol 85 (2) ◽  
pp. 998-1004 ◽  
Author(s):  
Martha J. Gdowski ◽  
Lee E. Miller ◽  
Todd Parrish ◽  
Emmanuel K. Nenonene ◽  
James C. Houk
Keyword(s):  
Globus Pallidus ◽  
Visual Cues ◽  
Discharge Rate ◽  
Context Dependency ◽  
Dependent Manner ◽  
Visually Guided ◽  
Single Neurons ◽  
Unit Discharge ◽  
Execution Unit ◽  
Globus Pallidus Internal

Extracellular discharges from single neurons in the internal segment of the globus pallidus (GPi) were recorded and analyzed for rate changes associated with visually guided forearm rotations to four different targets. We sought to examine how GPi neurons contribute to movement preparation and execution. Unit discharge from 108 GPi neurons recorded in 35 electrode penetrations was aligned to the time of various behavioral events, including the onset of cued and return movements. In total, 39 of 108 GPi neurons (36%) were task-modulated, demonstrating statistically significant changes in discharge rate at various times between the presentation of visual cues and movement generation. Most often, strong modulation in discharge rate occurred selectively during either the cued ( n = 32) or return ( n = 2) phases of the task, although a few neurons ( n = 5) were well-modulated during both movement phases. Of the 34 neurons that were modulated exclusively during cued or return movements, 50% ( n = 17) were modulated similarly in association with movements to any target. The remaining 17 neurons exhibited considerable diversity in their discharge properties associated with movements to each target. Cued phases of behavior were always rewarded if executed correctly, whereas return phases were never rewarded. Overall, these data reveal that many GPi neurons discharged in a context-dependent manner, being modulated during cued, rewarded movements, but not during similar self-paced, unrewarded movements. When considered in the light of other observations, the context-dependence we have observed seems likely to be influenced by the animal's expectation of reward.

Single-Unit Responses in the Inferior Colliculus of Decerebrate Cats II. Sensitivity to Interaural Level Differences

1999 ◽  
Vol 82 (1) ◽  
pp. 164-175 ◽  
Author(s):  
Kevin A. Davis ◽  
Ramnarayan Ramachandran ◽  
Bradford J. May
Keyword(s):  
Frequency Response ◽  
Inferior Colliculus ◽  
Free Field ◽  
Central Nucleus ◽  
Type I ◽  
Discharge Rates ◽  
Ipsilateral Stimulation ◽  
Interaural Level Differences ◽  
Type V ◽  
Decerebrate Cats

Single units in the central nucleus of the inferior colliculus (ICC) of unanesthetized decerebrate cats can be grouped into three distinct types (V, I, and O) according to the patterns of excitation and inhibition revealed in contralateral frequency response maps. This study extends the description of these response types by assessing their ipsilateral and binaural response map properties. Here the nature of ipsilateral inputs is evaluated directly using frequency response maps and compared with results obtained from methods that rely on sensitivity to interaural level differences (ILDs). In general, there is a one-to-one correspondence between observed ipsilateral input characteristics and those inferred from ILD manipulations. Type V units receive ipsilateral excitation and show binaural facilitation (EE properties); type I and type O units receive ipsilateral inhibition and show binaural excitatory/inhibitory (EI) interactions. Analyses of binaural frequency response maps show that these ILD effects extend over the entire receptive field of ICC units. Thus the range of frequencies that elicits excitation from type V units is expanded with increasing levels of ipsilateral stimulation, whereas the excitatory bandwidth of type I and O units decreases under the same binaural conditions. For the majority of ICC units, application of bicuculline, an antagonist for GABAA-mediated inhibition, does not alter the basic effects of binaural stimulation; rather, it primarily increases spontaneous and maximum discharge rates. These results support our previous interpretations of the putative dominant inputs to ICC response types and have important implications for midbrain processing of competing free-field sounds that reach the listener with different directional signatures.

Activity of single neurons in the monkey amygdala during performance of a visual discrimination task

1992 ◽  
Vol 67 (6) ◽  
pp. 1447-1463 ◽  
Author(s):  
K. Nakamura ◽  
A. Mikami ◽  
K. Kubota
Keyword(s):  
Visual Stimulus ◽  
Visual Discrimination ◽  
Discrimination Task ◽  
Discharge Rate ◽  
Visual Stimuli ◽  
Delay Period ◽  
Visual Discrimination Task ◽  
Single Neurons ◽  
Visual Neurons ◽  
Human Faces

1. The activity of single neurons was recorded extracellularly from the monkey amygdala while monkeys performed a visual discrimination task. The monkeys were trained to remember a visual stimulus during a delay period (0.5-3.0 s), to discriminate a new visual stimulus from the stimulus, and to release a lever when the new stimulus was presented. Colored photographs (human faces, monkeys, foods, and nonfood objects) or computer-generated two-dimensional shapes (a yellow triangle, a red circle, etc.) were used as visual stimuli. 2. The activity of 160 task-related neurons was studied. Of these, 144 (90%) responded to visual stimuli, 13 (8%) showed firing during the delay period, and 9 (6%) responded to the reward. 3. Task-related neurons were categorized according to the way in which various stimuli activated the neurons. First, to evaluate the proportion of all tested stimuli that elicited changes in activity of a neuron, selectivity index 1 (SI1) was employed. Second, to evaluate the ability of a neuron to discriminate a stimulus from another stimulus, SI2 was employed. On the basis of the calculated values of SI1 and SI2, neurons were classified as selective and nonselective. Most visual neurons were categorized as selective (131/144), and a few were characterized as nonselective (13/144). Neurons active during the delay period were also categorized as selective visual and delay neurons (6/13) and as nonselective delay neurons (7/13). 4. Responses of selective visual neurons had various temporal and stimulus-selective properties. Latencies ranged widely from 60 to 300 ms. Response durations also ranged widely from 20 to 870 ms. When the natures of the various effective stimuli were studied for each neuron, one-fourth of the responses of these neurons were considered to reflect some categorical aspect of the stimuli, such as human, monkey, food, or nonfood object. Furthermore, the responses of some neurons apparently reflected a certain behavioral significance of the stimuli that was separate from the task, such as the face of a particular person, smiling human faces, etc. 5. Nonselective visual neurons responded to a visual stimulus, regardless of its nature. They also responded in the absence of a visual stimulus when the monkey anticipated the appearance of the next stimulus. 6. Selective visual and delay neurons fired in response to particular stimuli and throughout the subsequent delay periods. Nonselective delay neurons increased their discharge rates gradually during the delay period, and the discharge rate decreased after the next stimulus was presented. 7. Task-related neurons were identified in six histologically distinct nuclei of the amygdala.(ABSTRACT TRUNCATED AT 400 WORDS)

Fast Inhibition Alters First Spike Timing in Auditory Brainstem Neurons

2004 ◽  
Vol 92 (4) ◽  
pp. 2615-2621 ◽  
Author(s):  
Antonio G. Paolini ◽  
Janine C. Clarey ◽  
Karina Needham ◽  
Graeme M. Clark
Keyword(s):  
Lateral Inhibition ◽  
Cochlear Nucleus ◽  
Stellate Cell ◽  
Discharge Rate ◽  
Stellate Cells ◽  
Auditory Pathway ◽  
Auditory Brainstem ◽  
Spike Timing ◽  
Inhibitory Neurons

Within the first processing site of the central auditory pathway, inhibitory neurons (D stellate cells) broadly tuned to tonal frequency project on narrowly tuned, excitatory output neurons (T stellate cells). The latter is thought to provide a topographic representation of sound spectrum, whereas the former is thought to provide lateral inhibition that improves spectral contrast, particularly in noise. In response to pure tones, the overall discharge rate in T stellate cells is unlikely to be suppressed dramatically by D stellate cells because they respond primarily to stimulus onset and provide fast, short-duration inhibition. In vivo intracellular recordings from the ventral cochlear nucleus (VCN) showed that, when tones were presented above or below the characteristic frequency (CF) of a T stellate neuron, they were inhibited during depolarization. This resulted in a delay in the initial action potential produced by T stellate cells. This ability of fast inhibition to alter the first spike timing of a T stellate neuron was confirmed by electrically activating the D stellate cell pathway that arises in the contralateral cochlear nucleus. Delay was also induced when two tones were presented: one at CF and one outside the frequency response area of the T stellate neuron. These findings suggest that the traditional view of lateral inhibition within the VCN should incorporate delay as one of its principle outcomes.

Binaural processing of sound pressure level in the inferior colliculus

1987 ◽  
Vol 57 (4) ◽  
pp. 1130-1147 ◽  
Author(s):  
M. N. Semple ◽  
L. M. Kitzes
Keyword(s):  
Inferior Colliculus ◽  
Sound Pressure ◽  
Spatial Information ◽  
Discharge Rate ◽  
Excitatory Input ◽  
Central Nucleus ◽  
Intensity Difference ◽  
Inhibitory Input ◽  
Directional Information ◽  
Discharge Rates

The central auditory system could encode information about the location of a high-frequency sound source by comparing the sound pressure levels at the ears. Two potential computations are the interaural intensity difference (IID) and the average binaural intensity (ABI). In this study of the central nucleus of the inferior colliculus (ICC) of the anesthetized gerbil, we demonstrate that responses of 85% of the 97 single units in our sample were jointly influenced by IID and ABI. For a given ABI, discharge rate of most units is a sigmoidal function of IID, and peak rates occur at IIDs favoring the contralateral ear. Most commonly, successive increments of ABI cause successive shifts of the IID functions toward IIDs favoring the ipsilateral ear. Neurons displaying this behavior include many that would conventionally be classified EI (receiving predominantly excitatory input arising from one ear and inhibitory input from the other), many that would be classified EE (receiving predominantly excitatory input arising from each ear), and all that are responsive only to contralateral stimulation. The IID sensitivity of a very few EI neurons is unaffected by ABI, except near threshold. Such units could provide directional information that is independent of source intensity. A few EE neurons are very sensitive to ABI, but are minimally sensitive to IID. Nevertheless, our data indicate that responses of most EE units in ICC are strongly dominated by excitation of contralateral origin. For some units, discharge rate is nonmonotonically related to IID and is maximal when the stimuli at the two ears are of comparable sound pressure. This preference for zero IID is common for all binaural levels. Many EI neurons respond nonmonotonically to ABI. Discharge rates are greater for IIDs representative of contralateral space and are maximal at a single best ABI. For a subset of these neurons, the influence arising from the ipsilateral ear is comprised of a mixture of excitation and inhibition. As a consequence, discharge rates are nonmonotonically related not only to ABI but also to IID. This dual nonmonotonicity creates a clear focus of peak response at a particular ABI/IID combination. Because of their mixed monaural influences, such units would be ascribed to different classes of the conventional (EE/EI) binaural classification scheme depending on the binaural level presented. Several response classes were identified in this study, and each might contribute differently to the encoding of spatial information.(ABSTRACT TRUNCATED AT 400 WORDS)

Effects of interaural time delays of noise stimuli on low-frequency cells in the cat's inferior colliculus. II. Responses to band-pass filtered noises

1987 ◽  
Vol 58 (3) ◽  
pp. 543-561 ◽  
Author(s):  
J. C. Chan ◽  
T. C. Yin ◽  
A. D. Musicant
Keyword(s):  
Inferior Colliculus ◽  
Time Delays ◽  
Discharge Rate ◽  
Low Frequency ◽  
Central Peak ◽  
Broadband Noise ◽  
Central Nucleus ◽  
Rate Curve ◽  
Median Frequency ◽  
Band Pass

1. We studied cells in the central nucleus of the inferior colliculus of the cat that were sensitive to interaural time delays (ITDs) in order to evaluate the influence of the stimulus spectrum of noise signals. Stimuli were sharply filtered low-, high-, and band-pass noise signals whose cutoff frequencies and bandwidths were systematically varied. The responses to ITDs of these noise signals were compared with responses obtained to ITDs of broadband noise and pure tones. 2. The discharge rate in response to band-pass noise as a function of ITD was usually a cyclic function with decreasing peak amplitudes at longer ITDs. The reciprocal of the mean interval between adjacent peaks indicated how rapidly the response rate varied with ITD and was termed the response frequency (RF). This RF was approximately equal to the median frequency of the stimulus spectrum filtered by the cell's sync-rate curve, which was the product of the synchronization to interaural phase and the discharge rate plotted against frequency. This suggests that the RF was determined by all the spectral components in the stimulus that fell within the frequency range in which the cell's response was synchronized. The contribution of each component was proportional to the sync-rate for that frequency. 3. The central peak of the ITD function usually fell within the physiological range of ITDs (+/- 400 microseconds). The location of this peak did not vary significantly with changes in stimulus spectrum by comparison with responses to tones of different frequency. Its shape also remained constant, except for a decrease in width when high-frequency components within the range of the sync-rate curve were added to the stimulus. A few cells responded with a minimal discharge instead of a maximal near-zero ITD, and this central minimum had similar properties as the central peak. The amplitude of the secondary peaks of the ITD function decreased as the stimulus bandwidth that overlapped the sync-rate curve broadened. 4. The sum of the ITD functions to two band-pass signals was similar to that of a broadband signal whose spectrum was composed of the sum of the band-pass spectra. 5. From these binaural responses we could make inferences about the response characteristics of the monaural inputs to binaural neurons. We then verified these predictions by studying responses of low-frequency trapezoid body fibers to band-pass noises.

scholarly journals Low error discrimination using a correlated population code

2012 ◽  
Vol 108 (4) ◽  
pp. 1069-1088 ◽  
Author(s):  
Greg Schwartz ◽  
Jakob Macke ◽  
Dario Amodei ◽  
Hanlin Tang ◽  
Michael J. Berry
Keyword(s):  
Spatial Information ◽  
Ganglion Cells ◽  
Discrimination Performance ◽  
Spike Timing ◽  
Multiple Time ◽  
Entropy Model ◽  
Decoding Algorithms ◽  
Single Spike ◽  
Order Of Magnitude ◽  
Spike Latency

We explored the manner in which spatial information is encoded by retinal ganglion cell populations. We flashed a set of 36 shape stimuli onto the tiger salamander retina and used different decoding algorithms to read out information from a population of 162 ganglion cells. We compared the discrimination performance of linear decoders, which ignore correlation induced by common stimulation, with nonlinear decoders, which can accurately model these correlations. Similar to previous studies, decoders that ignored correlation suffered only a modest drop in discrimination performance for groups of up to ∼30 cells. However, for more realistic groups of 100+ cells, we found order-of-magnitude differences in the error rate. We also compared decoders that used only the presence of a single spike from each cell with more complex decoders that included information from multiple spike counts and multiple time bins. More complex decoders substantially outperformed simpler decoders, showing the importance of spike timing information. Particularly effective was the first spike latency representation, which allowed zero discrimination errors for the majority of shape stimuli. Furthermore, the performance of nonlinear decoders showed even greater enhancement compared with linear decoders for these complex representations. Finally, decoders that approximated the correlation structure in the population by matching all pairwise correlations with a maximum entropy model fit to all 162 neurons were quite successful, especially for the spike latency representation. Together, these results suggest a picture in which linear decoders allow a coarse categorization of shape stimuli, whereas nonlinear decoders, which take advantage of both correlation and spike timing, are needed to achieve high-fidelity discrimination.

Spatial Phase and the Temporal Structure of the Response to Gratings in V1

1998 ◽  
Vol 80 (2) ◽  
pp. 554-571 ◽  
Author(s):  
Jonathan D. Victor ◽  
Keith P. Purpura
Keyword(s):  
Spatial Frequency ◽  
Spike Train ◽  
Temporal Structure ◽  
Spike Timing ◽  
Dependent Manner ◽  
Data Set ◽  
Simple Cells ◽  
Complex Cells ◽  
Spatial Phase ◽  
Contrast Information

Victor, Jonathan D. and Keith P. Purpura. Spatial phase and the temporal structure of the response to gratings in V1. J. Neurophysiol. 80: 554–571, 1998. We recorded single-unit activity of 25 units in the parafoveal representation of macaque V1 to transient appearance of sinusoidal gratings. Gratings were systematically varied in spatial phase and in one or two of the following: contrast, spatial frequency, and orientation. Individual responses were compared based on spike counts, and also according to metrics sensitive to spike timing. For each metric, the extent of stimulus-dependent clustering of individual responses was assessed via the transmitted information, H. In nearly all data sets, stimulus-dependent clustering was maximal for metrics sensitive to the temporal pattern of spikes, typically with a precision of 25–50 ms. To focus on the interaction of spatial phase with other stimulus attributes, each data set was analyzed in two ways. In the “pooled phases” approach, the phase of the stimulus was ignored in the assessment of clustering, to yield an index H pooled. In the “individual phases” approach, clustering was calculated separately for each spatial phase and then averaged across spatial phases to yield an index H indiv. H pooled expresses the extent to which a spike train represents contrast, spatial frequency, or orientation in a manner which is not confounded by spatial phase (phase-independent representation), whereas H indiv expresses the extent to which a spike train represents one of these attributes, provided spatial phase is fixed (phase-dependent representation). Here, representation means that a stimulus attribute has a reproducible and systematic influence on individual responses, not a neural mechanism for decoding this influence. During the initial 100 ms of the response, contrast was represented in a phase-dependent manner by simple cells but primarily in a phase-independent manner by complex cells. As the response evolved, simple cell responses acquired phase-independent contrast information, whereas complex cells acquired phase-dependent contrast information. Simple cells represented orientation and spatial frequency in a primarily phase-dependent manner, but also they contained some phase-independent information in their initial response segment. Complex cells showed primarily phase-independent representation of orientation but primarily phase-dependent representation of spatial frequency. Joint representation of two attributes (contrast and spatial frequency, contrast and orientation, spatial frequency and orientation) was primarily phase dependent for simple cells, and primarily phase independent for complex cells. In simple and complex cells, the variability in the number of spikes elicited on each response was substantially greater than the expectations of a Poisson process. Although some of this variation could be attributed to the dependence of the response on the spatial phase of the grating, variability was still markedly greater than Poisson when the contribution of spatial phase to response variance was removed.

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