scholarly journals Receptive field dimensionality increases from the auditory midbrain to cortex

2012 ◽  
Vol 107 (10) ◽  
pp. 2594-2603 ◽  
Author(s):  
Craig A. Atencio ◽  
Tatyana O. Sharpee ◽  
Christoph E. Schreiner
Keyword(s):  
Inferior Colliculus ◽  
Receptive Fields ◽  
Primary Auditory Cortex ◽  
Single Stimulus ◽  
Response Patterns ◽  
Neural Responses ◽  
Temporal Response ◽  
Auditory Midbrain ◽  
Independent Components ◽  
Spectrotemporal Receptive Fields

In the primary auditory cortex, spectrotemporal receptive fields (STRFs) are composed of multiple independent components that capture the processing of disparate stimulus aspects by any given neuron. The origin of these multidimensional stimulus filters in the central auditory system is unknown. To determine whether multicomponent STRFs emerge prior to the forebrain, we recorded from single neurons in the main obligatory station of the auditory midbrain, the inferior colliculus. By comparing results of different spike-triggered techniques, we found that the neural responses in the inferior colliculus can be accounted for by a single stimulus filter. This was observed for all temporal response patterns, from strongly phasic to tonic. Our results reveal that spectrotemporal stimulus encoding undergoes a fundamental transformation along the auditory neuraxis, with the emergence of multidimensional receptive fields beyond the auditory midbrain.

Frequency-Modulation Encoding in the Primary Auditory Cortex of the Awake Owl Monkey

2007 ◽  
Vol 98 (4) ◽  
pp. 2182-2195 ◽  
Author(s):  
Craig A. Atencio ◽  
David T. Blake ◽  
Fabrizio Strata ◽  
Steven W. Cheung ◽  
Michael M. Merzenich ◽  
...  
Keyword(s):  
Auditory Cortex ◽  
World Monkey ◽  
Receptive Fields ◽  
Primary Auditory Cortex ◽  
Direction Selectivity ◽  
Neural Responses ◽  
Population Distributions ◽  
Spectrotemporal Receptive Fields ◽  
Owl Monkey ◽  
Highly Correlated

Many communication sounds, such as New World monkey twitter calls, contain frequency-modulated (FM) sweeps. To determine how this prominent vocalization element is represented in the auditory cortex we examined neural responses to logarithmic FM sweep stimuli in the primary auditory cortex (AI) of two awake owl monkeys. Using an implanted array of microelectrodes we quantitatively characterized neuronal responses to FM sweeps and to random tone-pip stimuli. Tone-pip responses were used to construct spectrotemporal receptive fields (STRFs). Classification of FM sweep responses revealed few neurons with high direction and speed selectivity. Most neurons responded to sweeps in both directions and over a broad range of sweep speeds. Characteristic frequency estimates from FM responses were highly correlated with estimates from STRFs, although spectral receptive field bandwidth was consistently underestimated by FM stimuli. Predictions of FM direction selectivity and best speed from STRFs were significantly correlated with observed FM responses, although some systematic discrepancies existed. Last, the population distributions of FM responses in the awake owl monkey were similar to, although of longer temporal duration than, those in the anesthetized squirrel monkeys.

scholarly journals Passive stimulation and behavioral training differentially transform temporal processing in the inferior colliculus and primary auditory cortex

2017 ◽  
Vol 117 (1) ◽  
pp. 47-64 ◽  
Author(s):  
Maike Vollmer ◽  
Ralph E. Beitel ◽  
Christoph E. Schreiner ◽  
Patricia A. Leake
Keyword(s):  
Auditory Cortex ◽  
Inferior Colliculus ◽  
Temporal Processing ◽  
Electric Stimulation ◽  
Primary Auditory Cortex ◽  
Central Nucleus ◽  
Electrophysiological Recording ◽  
Response Patterns ◽  
Behavioral Training ◽  
Auditory Midbrain

In profoundly deaf cats, behavioral training with intracochlear electric stimulation (ICES) can improve temporal processing in the primary auditory cortex (AI). To investigate whether similar effects are manifest in the auditory midbrain, ICES was initiated in neonatally deafened cats either during development after short durations of deafness (8 wk of age) or in adulthood after long durations of deafness (≥3.5 yr). All of these animals received behaviorally meaningless, “passive” ICES. Some animals also received behavioral training with ICES. Two long-deaf cats received no ICES prior to acute electrophysiological recording. After several months of passive ICES and behavioral training, animals were anesthetized, and neuronal responses to pulse trains of increasing rates were recorded in the central (ICC) and external (ICX) nuclei of the inferior colliculus. Neuronal temporal response patterns (repetition rate coding, minimum latencies, response precision) were compared with results from recordings made in the AI of the same animals (Beitel RE, Vollmer M, Raggio MW, Schreiner CE. J Neurophysiol 106: 944–959, 2011; Vollmer M, Beitel RE. J Neurophysiol 106: 2423–2436, 2011). Passive ICES in long-deaf cats remediated severely degraded temporal processing in the ICC and had no effects in the ICX. In contrast to observations in the AI, behaviorally relevant ICES had no effects on temporal processing in the ICC or ICX, with the single exception of shorter latencies in the ICC in short-deaf cats. The results suggest that independent of deafness duration passive stimulation and behavioral training differentially transform temporal processing in auditory midbrain and cortex, and primary auditory cortex emerges as a pivotal site for behaviorally driven neuronal temporal plasticity in the deaf cat. NEW & NOTEWORTHY Behaviorally relevant vs. passive electric stimulation of the auditory nerve differentially affects neuronal temporal processing in the central nucleus of the inferior colliculus (ICC) and the primary auditory cortex (AI) in profoundly short-deaf and long-deaf cats. Temporal plasticity in the ICC depends on a critical amount of electric stimulation, independent of its behavioral relevance. In contrast, the AI emerges as a pivotal site for behaviorally driven neuronal temporal plasticity in the deaf auditory system.

scholarly journals Spectral and Temporal Modulation Tradeoff in the Inferior Colliculus

2010 ◽  
Vol 103 (2) ◽  
pp. 887-903 ◽  
Author(s):  
Francisco A. Rodríguez ◽  
Heather L. Read ◽  
Monty A. Escabí
Keyword(s):  
Inferior Colliculus ◽  
Spectral Characteristics ◽  
Receptive Fields ◽  
Nerve Fibers ◽  
Central Nucleus ◽  
Natural Sounds ◽  
Auditory Midbrain ◽  
Spectrotemporal Receptive Fields ◽  
Low Pass ◽  
Frequency Selective Channels

The cochlea encodes sounds through frequency-selective channels that exhibit low-pass modulation sensitivity. Unlike the cochlea, neurons in the auditory midbrain are tuned for spectral and temporal modulations found in natural sounds, yet the role of this transformation is not known. We report a distinct tradeoff in modulation sensitivity and tuning that is topographically ordered within the central nucleus of the inferior colliculus (CNIC). Spectrotemporal receptive fields (STRFs) were obtained with 16-channel electrodes inserted orthogonal to the isofrequency lamina. Surprisingly, temporal and spectral characteristics exhibited an opposing relationship along the tonotopic axis. For low best frequencies (BFs), units were selective for fast temporal and broad spectral modulations. A systematic progression was observed toward slower temporal and finer spectral modulation sensitivity at high BF. This tradeoff was strongly reflected in the arrangement of excitation and inhibition and, consequently, in the modulation tuning characteristics. Comparisons with auditory nerve fibers show that these trends oppose the pattern imposed by the peripheral filters. These results suggest that spectrotemporal preferences are reordered within the tonotopic axis of the CNIC. This topographic organization has profound implications for the coding of spectrotemporal features in natural sounds and could underlie a number of perceptual phenomena.

scholarly journals Role of the Zebra Finch Auditory Thalamus in Generating Complex Representations for Natural Sounds

2010 ◽  
Vol 104 (2) ◽  
pp. 784-798 ◽  
Author(s):  
Noopur Amin ◽  
Patrick Gill ◽  
Frédéric E. Theunissen
Keyword(s):  
Receptive Fields ◽  
Neural Representation ◽  
Natural Sounds ◽  
Auditory Midbrain ◽  
Complex Sounds ◽  
Auditory Thalamus ◽  
Spectrotemporal Receptive Fields ◽  
Primary Sensory Cortex ◽  
Relay Nucleus ◽  
Field L

We estimated the spectrotemporal receptive fields of neurons in the songbird auditory thalamus, nucleus ovoidalis, and compared the neural representation of complex sounds in the auditory thalamus to those found in the upstream auditory midbrain nucleus, mesencephalicus lateralis dorsalis (MLd), and the downstream auditory pallial region, field L. Our data refute the idea that the primary sensory thalamus acts as a simple, relay nucleus: we find that the auditory thalamic receptive fields obtained in response to song are more complex than the ones found in the midbrain. Moreover, we find that linear tuning diversity and complexity in ovoidalis (Ov) are closer to those found in field L than in MLd. We also find prevalent tuning to intermediate spectral and temporal modulations, a feature that is unique to Ov. Thus even a feed-forward model of the sensory processing chain, where neural responses in the sensory thalamus reveals intermediate response properties between those in the sensory periphery and those in the primary sensory cortex, is inadequate in describing the tuning found in Ov. Based on these results, we believe that the auditory thalamic circuitry plays an important role in generating novel complex representations for specific features found in natural sounds.

scholarly journals Anesthetic state modulates excitability but not spectral tuning or neural discrimination in single auditory midbrain neurons

2011 ◽  
Vol 106 (2) ◽  
pp. 500-514 ◽  
Author(s):  
Joseph W. Schumacher ◽  
David M. Schneider ◽  
Sarah M. N. Woolley
Keyword(s):  
Receptive Fields ◽  
Population Level ◽  
Sensory Function ◽  
Spectral Tuning ◽  
Auditory Midbrain ◽  
Sensory Physiology ◽  
Neural Excitability ◽  
Midbrain Neurons ◽  
Spectrotemporal Receptive Fields

The majority of sensory physiology experiments have used anesthesia to facilitate the recording of neural activity. Current techniques allow researchers to study sensory function in the context of varying behavioral states. To reconcile results across multiple behavioral and anesthetic states, it is important to consider how and to what extent anesthesia plays a role in shaping neural response properties. The role of anesthesia has been the subject of much debate, but the extent to which sensory coding properties are altered by anesthesia has yet to be fully defined. In this study we asked how urethane, an anesthetic commonly used for avian and mammalian sensory physiology, affects the coding of complex communication vocalizations (songs) and simple artificial stimuli in the songbird auditory midbrain. We measured spontaneous and song-driven spike rates, spectrotemporal receptive fields, and neural discriminability from responses to songs in single auditory midbrain neurons. In the same neurons, we recorded responses to pure tone stimuli ranging in frequency and intensity. Finally, we assessed the effect of urethane on population-level representations of birdsong. Results showed that intrinsic neural excitability is significantly depressed by urethane but that spectral tuning, single neuron discriminability, and population representations of song do not differ significantly between unanesthetized and anesthetized animals.

Spectrotemporal Structure of Receptive Fields in Areas AI and AAF of Mouse Auditory Cortex

2003 ◽  
Vol 90 (4) ◽  
pp. 2660-2675 ◽  
Author(s):  
Jennifer F. Linden ◽  
Robert C. Liu ◽  
Maneesh Sahani ◽  
Christoph E. Schreiner ◽  
Michael M. Merzenich
Keyword(s):  
Receptive Field ◽  
Auditory Cortex ◽  
Receptive Fields ◽  
Primary Auditory Cortex ◽  
Dynamic Stimuli ◽  
Tuning Curves ◽  
Response Characteristics ◽  
Spectrotemporal Receptive Fields ◽  
Auditory Field ◽  
Tonal Stimuli

The mouse is a promising model system for auditory cortex research because of the powerful genetic tools available for manipulating its neural circuitry. Previous studies have identified two tonotopic auditory areas in the mouse—primary auditory cortex (AI) and anterior auditory field (AAF)— but auditory receptive fields in these areas have not yet been described. To establish a foundation for investigating auditory cortical circuitry and plasticity in the mouse, we characterized receptive-field structure in AI and AAF of anesthetized mice using spectrally complex and temporally dynamic stimuli as well as simple tonal stimuli. Spectrotemporal receptive fields (STRFs) were derived from extracellularly recorded responses to complex stimuli, and frequency-intensity tuning curves were constructed from responses to simple tonal stimuli. Both analyses revealed temporal differences between AI and AAF responses: peak latencies and receptive-field durations for STRFs and first-spike latencies for responses to tone bursts were significantly longer in AI than in AAF. Spectral properties of AI and AAF receptive fields were more similar, although STRF bandwidths were slightly broader in AI than in AAF. Finally, in both AI and AAF, a substantial minority of STRFs were spectrotemporally inseparable. The spectrotemporal interaction typically appeared in the form of clearly disjoint excitatory and inhibitory subfields or an obvious spectrotemporal slant in the STRF. These data provide the first detailed description of auditory receptive fields in the mouse and suggest that although neurons in areas AI and AAF share many response characteristics, area AAF may be specialized for faster temporal processing.

scholarly journals Laminar Diversity of Dynamic Sound Processing in Cat Primary Auditory Cortex

2010 ◽  
Vol 103 (1) ◽  
pp. 192-205 ◽  
Author(s):  
Craig A. Atencio ◽  
Christoph E. Schreiner
Keyword(s):  
Auditory Cortex ◽  
Transfer Functions ◽  
Receptive Fields ◽  
Primary Auditory Cortex ◽  
Functional Characteristic ◽  
Modulation Transfer ◽  
Spectral Modulation ◽  
Spectrotemporal Receptive Fields ◽  
Low Pass ◽  
Acoustic Modulation

For primary auditory cortex (AI) laminae, there is little evidence of functional specificity despite clearly expressed cellular and connectional differences. Natural sounds are dominated by dynamic temporal and spectral modulations and we used these properties to evaluate local functional differences or constancies across laminae. To examine the layer-specific processing of acoustic modulation information, we simultaneously recorded from multiple AI laminae in the anesthetized cat. Neurons were challenged with dynamic moving ripple stimuli and we subsequently computed spectrotemporal receptive fields (STRFs). From the STRFs, temporal and spectral modulation transfer functions (tMTFs, sMTFs) were calculated and compared across layers. Temporal and spectral modulation properties often differed between layers. On average, layer II/III and VI neurons responded to lower temporal modulations than those in layer IV. tMTFs were mainly band-pass in granular layer IV and became more low-pass in infragranular layers. Compared with layer IV, spectral MTFs were broader and their upper cutoff frequencies higher in layers V and VI. In individual penetrations, temporal modulation preference was similar across layers for roughly 70% of the penetrations, suggesting a common, columnar functional characteristic. By contrast, only about 30% of penetrations showed consistent spectral modulation preferences across layers, indicative of functional laminar diversity or specialization. Since local laminar differences in stimulus preference do not always parallel the main flow of information in the columnar cortical microcircuit, this indicates the influence of additional horizontal or thalamocortical inputs. AI layers that express differing modulation properties may serve distinct roles in the extraction of dynamic sound information, with the differing information specific to the targeted stations of each layer.

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