Affects of Aging on Receptive Fields in Rat Primary Auditory Cortex Layer V Neurons

2005 ◽  
Vol 94 (4) ◽  
pp. 2738-2747 ◽  
Author(s):  
Jeremy G. Turner ◽  
Larry F. Hughes ◽  
Donald M. Caspary
Keyword(s):  
Receptive Field ◽  
Auditory Cortex ◽  
Receptive Fields ◽  
Primary Auditory Cortex ◽  
Brown Norway ◽  
Aged Rats ◽  
Adult Rats ◽  
Gabaergic Neurotransmission ◽  
Layer V

Advanced age is commonly associated with progressive cochlear pathology and central auditory deficits, collectively known as presbycusis. The present study examined central correlates of presbycusis by measuring response properties of primary auditory cortex (AI) layer V neurons in the Fischer Brown Norway rat model. Layer V neurons represent the major output of AI to other cortical and subcortical regions (primarily the inferior colliculus). In vivo single-unit extracellular recordings were obtained from 114 neurons in aged animals (29–33 mo) and compared with 105 layer V neurons in young-adult rats (4–6 mo). Three consecutive repetitions of a pure-tone receptive field map were run for each neuron. Age was associated with fewer neurons exhibiting classic V/U-shaped receptive fields and a greater percentage of neurons with more Complex receptive fields. Receptive fields from neurons in aged rats were also less reliable on successive repetitions of the same stimulus set. Aging was also associated with less firing during the stimulus in V/U-shaped receptive field neurons and more firing during the stimulus in Complex neurons, which were generally associated with inhibited firing in young controls. Finally, neurons in aged rats with Complex receptive fields were more easily driven by current pulses delivered to the soma. Collectively, these findings provide support for the notion that age is associated with diminished signal-to-noise coding by AI layer V neurons and are consistent with other research suggesting that GABAergic neurotransmission in AI may be compromised by aging.

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.

Intracortical Pathways Determine Breadth of Subthreshold Frequency Receptive Fields in Primary Auditory Cortex

2004 ◽  
Vol 91 (6) ◽  
pp. 2551-2567 ◽  
Author(s):  
Simranjit Kaur ◽  
Ronit Lazar ◽  
Raju Metherate
Keyword(s):  
Receptive Field ◽  
Auditory Cortex ◽  
Receptive Fields ◽  
Field Potential ◽  
Primary Auditory Cortex ◽  
Response Threshold ◽  
Complex Stimuli ◽  
Cortical Receptive Fields ◽  
Local Field Potential Lfp ◽  
Integrated Responses

To examine the basis of frequency receptive fields in auditory cortex (ACx), we have recorded intracellular (whole cell) and extracellular (local field potential, LFP) responses to tones in anesthetized rats. Frequency receptive fields derived from excitatory postsynaptic potentials (EPSPs) and LFPs from the same location resembled each other in terms of characteristic frequency (CF) and breadth of tuning, suggesting that LFPs reflect local synaptic (including subthreshold) activity. Subthreshold EPSP and LFP receptive fields were remarkably broad, often spanning five octaves (the maximum tested) at moderate intensities (40–50 dB above threshold). To identify receptive-field features that are generated intracortically, we microinjected the GABAA receptor agonist muscimol (0.2–5.1 mM, 1–5 μl) into ACx. Muscimol dramatically reduced LFP amplitude and reduced receptive-field bandwidth, implicating intracortical contributions to these features but had lesser effects on CF response threshold or onset latency, suggesting minimal loss of thalamocortical input. Reversal of muscimol's inhibition preferentially at the recording site by diffusion from the recording pipette of the GABAA receptor antagonist picrotoxin (0.01–100 μM) disinhibited responses to CF stimuli more than responses to spectrally distant, non-CF stimuli. We propose that thalamocortical and intracortical pathways preferentially contribute to responses evoked by CF and non-CF stimuli, respectively, and that intracortical projections linking frequency representations determine the breadth of receptive fields in primary ACx. Broad, subthreshold receptive fields may distinguish ACx from subcortical auditory relay nuclei, promote integrated responses to spectrotemporally complex stimuli, and provide a substrate for plasticity of cortical receptive fields and maps.

scholarly journals Stimulus-specific adaptation in auditory thalamus of young and aged awake rats

2013 ◽  
Vol 110 (8) ◽  
pp. 1892-1902 ◽  
Author(s):  
Ben D. Richardson ◽  
Kenneth E. Hancock ◽  
Donald M. Caspary
Keyword(s):  
Young Adult ◽  
Auditory Cortex ◽  
Brown Norway ◽  
Oddball Paradigm ◽  
Adult Rats ◽  
Specific Adaptation ◽  
Auditory Thalamus ◽  
Gating Mechanism ◽  
Medial Geniculate ◽  
Awake Rats

Novel stimulus detection by single neurons in the auditory system, known as stimulus-specific adaptation (SSA), appears to function as a real-time filtering/gating mechanism in processing acoustic information. Particular stimulus paradigms allowing for quantification of a neuron's ability to detect novel or deviant stimuli have been used to examine SSA in the inferior colliculus, medial geniculate body (MGB), and auditory cortex of anesthetized rodents. However, the study of SSA in awake animals is limited to auditory cortex. The present study used individually advanceable tetrodes to record single-unit responses from auditory thalamus (MGB) of awake young adult and aged Fischer Brown Norway (FBN) rats to 1) examine the presence of SSA in the MGB of awake rats and 2) determine whether SSA is altered by aging in MGB. MGB single units in awake FBN rats displayed SSA in response to two stimulus paradigms: the oddball paradigm and a random blocked/interleaved presentation of a set of frequencies. SSA levels were modestly, but nonsignificantly, increased in the nonlemniscal regions of the MGB and at lower stimulus intensities, where 27 of 57 (47%) young adult MGB units displayed SSA. The present findings provide the initial description of SSA in the MGB of awake rats and support SSA as being qualitatively independent of arousal level or anesthetized state. Finally, contrary to previous studies in auditory cortex of anesthetized rats, MGB units in aged rats showed SSA levels indistinguishable from SSA levels in young adult rats, suggesting that SSA in MGB was not impacted by aging in an awake preparation.

Heterogeneous Neuronal Responses to Frequency-Modulated Tones in the Primary Auditory Cortex of Awake Cats

2008 ◽  
Vol 100 (3) ◽  
pp. 1622-1634 ◽  
Author(s):  
Ling Qin ◽  
JingYu Wang ◽  
Yu Sato
Keyword(s):  
Receptive Field ◽  
Auditory Cortex ◽  
Response Pattern ◽  
Primary Auditory Cortex ◽  
Neuronal Responses ◽  
Discrete Response ◽  
A Cell ◽  
Pure Tones ◽  
Awake Cats ◽  
Sweep Speed

Previous studies in anesthetized animals reported that the primary auditory cortex (A1) showed homogenous phasic responses to FM tones, namely a transient response to a particular instantaneous frequency when FM sweeps traversed a neuron's tone-evoked receptive field (TRF). Here, in awake cats, we report that A1 cells exhibit heterogeneous FM responses, consisting of three patterns. The first is continuous firing when a slow FM sweep traverses the receptive field of a cell with a sustained tonal response. The duration and amplitude of FM response decrease with increasing sweep speed. The second pattern is transient firing corresponding to the cell's phasic tonal response. This response could be evoked only by a fast FM sweep through the cell's TRF, suggesting a preference for fast FM. The third pattern was associated with the off response to pure tones and was composed of several discrete response peaks during slow FM stimulus. These peaks were not predictable from the cell's tonal response but reliably reflected the time when FM swept across specific frequencies. Our A1 samples often exhibited a complex response pattern, combining two or three of the basic patterns above, resulting in a heterogeneous response population. The diversity of FM responses suggests that A1 use multiple mechanisms to fully represent the whole range of FM parameters, including frequency extent, sweep speed, and direction.

scholarly journals Pairing Cholinergic Enhancement with Perceptual Training Promotes Recovery of Age-Related Changes in Rat Primary Auditory Cortex

2016 ◽  
Vol 2016 ◽  
pp. 1-18 ◽  
Author(s):  
Patrice Voss ◽  
Maryse Thomas ◽  
You Chien Chou ◽  
José Miguel Cisneros-Franco ◽  
Lydia Ouellet ◽  
...  
Keyword(s):  
Auditory Cortex ◽  
Structural Changes ◽  
Primary Auditory Cortex ◽  
Auditory Training ◽  
Tone Frequency ◽  
Perceptual Training ◽  
Adult Rats ◽  
Functional Changes ◽  
Age Related ◽  
Old Rats

We used the rat primary auditory cortex (A1) as a model to probe the effects of cholinergic enhancement on perceptual learning and auditory processing mechanisms in both young and old animals. Rats learned to perform a two-tone frequency discrimination task over the course of two weeks, combined with either the administration of a cholinesterase inhibitor or saline. We found that while both age groups learned the task more quickly through cholinergic enhancement, the young did so by improving target detection, whereas the old did so by inhibiting erroneous responses to nontarget stimuli. We also found that cholinergic enhancement led to marked functional and structural changes within A1 in both young and old rats. Importantly, we found that several functional changes observed in the old rats, particularly those relating to the processing and inhibition of nontargets, produced cortical processing features that resembled those of young untrained rats more so than those of older adult rats. Overall, these findings demonstrate that combining auditory training with neuromodulation of the cholinergic system can restore many of the auditory cortical functional deficits observed as a result of normal aging and add to the growing body of evidence demonstrating that many age-related perceptual and neuroplastic changes are reversible.

Disruption of Balanced Cortical Excitation and Inhibition by Acoustic Trauma

2008 ◽  
Vol 100 (2) ◽  
pp. 646-656 ◽  
Author(s):  
Ben Scholl ◽  
Michael Wehr
Keyword(s):  
Receptive Field ◽  
Cortical Neurons ◽  
Receptive Fields ◽  
Acoustic Trauma ◽  
Tone Frequency ◽  
Synaptic Excitation ◽  
Before And After ◽  
High Level ◽  
Whole Cell Recordings

Sensory deafferentation results in rapid shifts in the receptive fields of cortical neurons, but the synaptic mechanisms underlying these changes remain unknown. The rapidity of these shifts has led to the suggestion that subthreshold inputs may be unmasked by a selective loss of inhibition. To study this, we used in vivo whole cell recordings to directly measure tone-evoked excitatory and inhibitory synaptic inputs in auditory cortical neurons before and after acoustic trauma. Here we report that acute acoustic trauma disrupted the balance of excitation and inhibition by selectively increasing and reducing the strength of inhibition at different positions within the receptive field. Inhibition was abolished for frequencies far below the trauma-tone frequency but was markedly enhanced near the edges of the region of elevated peripheral threshold. These changes occurred for relatively high-level tones. These changes in inhibition led to an expansion of receptive fields but not by a simple unmasking process. Rather, membrane potential responses were delayed and prolonged throughout the receptive field by distinct interactions between synaptic excitation and inhibition. Far below the trauma-tone frequency, decreased inhibition combined with prolonged excitation led to increased responses. Near the edges of the region of elevated peripheral threshold, increased inhibition served to delay rather than abolish responses, which were driven by prolonged excitation. These results show that the rapid receptive field shifts caused by acoustic trauma are caused by distinct mechanisms at different positions within the receptive field, which depend on differential disruption of excitation and inhibition.

Delayed Inhibition in Cortical Receptive Fields and the Discrimination of Complex Stimuli

2005 ◽  
Vol 94 (4) ◽  
pp. 2970-2975 ◽  
Author(s):  
Rajiv Narayan ◽  
Ayla Ergün ◽  
Kamal Sen
Keyword(s):  
Auditory Cortex ◽  
Temporal Structure ◽  
Receptive Fields ◽  
Primary Auditory Cortex ◽  
Natural Sounds ◽  
Functional Roles ◽  
Complex Stimuli ◽  
Animal Vocalizations ◽  
Field L ◽  
Cortical Receptive Fields

Although auditory cortex is thought to play an important role in processing complex natural sounds such as speech and animal vocalizations, the specific functional roles of cortical receptive fields (RFs) remain unclear. Here, we study the relationship between a behaviorally important function: the discrimination of natural sounds and the structure of cortical RFs. We examine this problem in the model system of songbirds, using a computational approach. First, we constructed model neurons based on the spectral temporal RF (STRF), a widely used description of auditory cortical RFs. We focused on delayed inhibitory STRFs, a class of STRFs experimentally observed in primary auditory cortex (ACx) and its analog in songbirds (field L), which consist of an excitatory subregion and a delayed inhibitory subregion cotuned to a characteristic frequency. We quantified the discrimination of birdsongs by model neurons, examining both the dynamics and temporal resolution of discrimination, using a recently proposed spike distance metric (SDM). We found that single model neurons with delayed inhibitory STRFs can discriminate accurately between songs. Discrimination improves dramatically when the temporal structure of the neural response at fine timescales is considered. When we compared discrimination by model neurons with and without the inhibitory subregion, we found that the presence of the inhibitory subregion can improve discrimination. Finally, we modeled a cortical microcircuit with delayed synaptic inhibition, a candidate mechanism underlying delayed inhibitory STRFs, and showed that blocking inhibition in this model circuit degrades discrimination.

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