Divergent response properties of layer-V neurons in rat primary auditory cortex

Turner, Jeremy G.; Hughes, Larry F.; Caspary, Donald M.

doi:10.1016/j.heares.2004.09.011

Cited by 31 publications

(29 citation statements)

References 65 publications

(74 reference statements)

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“…FRA maps with multiple patterns have also been reported in the past. For example, Turner et al (2005) showed some neurons with complex, intermediate, and high-threshold FRA maps in layer V of the rat A1, which is in agreement with the FRA maps latterly noted by Sakata and Harris (2009) for PCs and INs in other cortical layers of the rat A1. Neurons with separated subregions in their FRA maps, besides classical V-shaped tuning, have also been found (Gaese and Ostwald, 2003).…”

Section: Discussionsupporting

confidence: 86%

“…The existence of nonclassical schemes may be in line with findings reported recently: (1) complex FRA maps (Schreiner et al, 2000;Gaese and Ostwald, 2003;Turner et al, 2005); (2) inhibitory sideband effects (O'Connell et al, 2011); (3) high variability along cortical layers (Wallace and Palmer, 2008;Sakata and Harris, 2009;Hackett et al, 2011); and (4) sparseness activation patterns (Hromádka et al, 2008;Sakata and Harris, 2009;Rothschild et al, 2010). Therefore, to study the neuronal substrates for sound attribute codification in A1 of Wistar rats, we chose to apply a simple but complementary approach that is based on a massive exploration of a large cortical sheet at all depths.…”

Section: Introductionsupporting

confidence: 91%

“…6, top). The most abundant type was the positive slope codifier, which may consist of neurons with high-pass tuning patterns similar to those reported in the past (Turner et al, 2005;Sakata and Harris, 2009). Second, to reproduce the classic tonotopic organization in the sense of neuronal populations, for each carrier frequency f c , we calculated the mean of the spiking rate resulting from integrating the other two conditions (i.e., modulation frequency f m and amplitude Amp).…”

Section: Spatial Aggregation/segregation Of Attribute Codifiersmentioning

confidence: 99%

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Large-Scale Heterogeneous Representation of Sound Attributes in Rat Primary Auditory Cortex: From Unit Activity to Population Dynamics

Ogawa¹,

Riera²,

Goto³

et al. 2011

J. Neurosci.

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Recent evidence indicates the existence of pyramidal cells (PCs) and interneurons with nontrivial tuning characteristics for sound attributes in the primary auditory cortex (A1) of mammals. These neurons are functionally distributed into layers and sparsely organized at a small scale. However, their topological locations at a large scale in A1 have not yet been investigated. Furthermore, these neurons are usually classified from fine maps of attribute-dependent spiking activity, and not much attention is paid to population postsynaptic potentials related to their activity. We used extracellular recordings obtained from multiple sites in A1 of adult rats to determine neuronal codifiers for sound attributes defined by coarse representations of the population dose-response curves. We demonstrated that these codifiers, majorly involving PCs, are heterogeneously distributed along A1. Spiking activity in these neurons during stimulation was correlated to ␤ (12-25 Hz) and low ␥ (25-70 Hz) postsynaptic oscillations in the infragranular layer, whereas in the supragranular layer, better correlations were found with high ␥ (70 -170 Hz) oscillations. The time-frequency analysis of the postsynaptic potentials showed a transient broadband power increase in all layers after the stimulus onset that was followed by a sustained high ␥ oscillation in the supragranular layer, fluctuations in the laminar content of the low-frequency oscillations, and a global attenuation in the low-frequency powers after the stimulus offset that happened together with a long-lasting strengthening of the ␤ oscillations. We concluded that, for rats, sounds are codified in A1 by segregated networks of specialized PCs whose postsynaptic activity impinges on the emergence of sparse/dense spiking patterns.

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Section: Discussionsupporting

confidence: 86%

Section: Introductionsupporting

confidence: 91%

Section: Spatial Aggregation/segregation Of Attribute Codifiersmentioning

confidence: 99%

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Large-Scale Heterogeneous Representation of Sound Attributes in Rat Primary Auditory Cortex: From Unit Activity to Population Dynamics

Ogawa¹,

Riera²,

Goto³

et al. 2011

J. Neurosci.

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“…Fourth, aging in Complex receptive field maps, but not V/U maps, was associated with an increased discharge rate in response to extracellular current pulse stimulation (Fig. 5C).The two major divergent receptive field shapes clearly code sounds differently and are thought to convey different stimulus information (Turner et al, 2005a;Turner et al, 2005b) and are likely to have distinctly different projection patterns (Hefti and Smith, 2000;Hefti and Smith, 2003). V/U-shaped receptive field neurons are more closely associated with larger pyramidal cells that form the descending projections to the brainstem (Games and Winer, 1988;Winer et al, 1998;Winer and Prieto, 2001;Turner et al, 2005a).…”

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confidence: 93%

Inhibitory neurotransmission, plasticity and aging in the mammalian central auditory system

Caspary

Ling

Turner

et al. 2008

Journal of Experimental Biology

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429

355

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SummaryAging and acoustic trauma may result in partial peripheral deafferentation in the central auditory pathway of the mammalian brain. In accord with homeostatic plasticity, loss of sensory input results in a change in pre-and postsynaptic GABAergic and glycinergic inhibitory neurotransmission. As seen in development, age-related changes may be activity dependent. Age-related presynaptic changes in the cochlear nucleus include reduced glycine levels, while in the auditory midbrain and cortex, GABA synthesis and release are altered. Presumably, in response to age-related decreases in presynaptic release of inhibitory neurotransmitters, there are age-related postsynaptic subunit changes in the composition of the glycine (GlyR) and GABA A (GABA A R) receptors. Age-related changes in the subunit makeup of inhibitory pentameric receptor constructs result in altered pharmacological and physiological responses consistent with a net down-regulation of functional inhibition. Age-related functional changes associated with glycine neurotransmission in dorsal cochlear nucleus (DCN) include altered intensity and temporal coding by DCN projection neurons. Loss of synaptic inhibition in the superior olivary complex (SOC) and the inferior colliculus (IC) likely affect the ability of aged animals to localize sounds in their natural environment. Age-related postsynaptic GABA A R changes in IC and primary auditory cortex (A1) involve changes in the subunit makeup of GABA A Rs. In turn, these changes cause age-related changes in the pharmacology and response properties of neurons in IC and A1 circuits, which collectively may affect temporal processing and response reliability. Findings of age-related inhibitory changes within mammalian auditory circuits are similar to age and deafferentation plasticity changes observed in other sensory systems. Although few studies have examined sensory aging in the wild, these age-related changes would likely compromise an animal's ability to avoid predation or to be a successful predator in their natural environment.Key words: aging, central auditory system, GABA A receptor, glycine receptor, inhibitory neurotransmission, plasticity. THE JOURNAL OF EXPERIMENTAL BIOLOGY 1782important in determining the location of sound, echolocation and extracting information from voiced and unvoiced communication signals (Carr et al., 1986;Portfors and Wenstrup, 2001).The complex processing that occurs at the level of the MGB and the A1 is beyond the scope of the present review. Coding in the auditory cortex has been recently reviewed (Wang, 2007;Rauschecker, 2005). As seen in the visual cortex, in the auditory cortex, acoustically complex hierarchical analysis has been described for awake-behaving primates (Rauschecker, 2005;Steinschneider et al., 2008). A1 has been shown to undergo agerelated plastic changes, including down-regulation of inhibitory coding, similar to that observed at lower levels of the auditory pathway and in visual cortex. Similar to age-related changes, activity-dependant changes have be...

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“…Anesthesia was maintained by alternating hourly boosters of ketamine alone (~33 mg/kg) or ketamine/xylazine mixture (approximately one-third the original dose). Aged rats received lower doses of anesthesia (~85% of the young animal doses) to compensate for reduced liver function (Finlayson and Caspary, 1993;Palombi and Caspary, 1996;Turner et al, 2005). Booster times were similar for young and aged FBN rats suggesting that the dose adjustment for aged animals was appropriate.…”

Section: Experimental Procedures Surgical Protocolmentioning

confidence: 99%

Aged-related loss of temporal processing: Altered responses to amplitude modulated tones in rat dorsal cochlear nucleus

2008

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Loss of temporal processing is characteristic of age-related loss of speech understanding observed in the elderly. Inhibitory glycinergic circuits provide input onto dorsal cochlear nucleus (DCN) projection neurons which likely serve to modulate excitatory responses to time-varying complex acoustic signals. The present study sought to test the hypothesis that age-related loss of inhibition would compromise the ability of output neurons to encode sinusoidally amplitude modulated (SAM) tones. Extracellular recordings were obtained from young and aged FBN rat DCN putative fusiform cells. Stimuli were SAM tones at 3 modulation depths (100, 50, and 20%) at 30 dB HL with the carrier frequency set to the unit's characteristic frequency. Discharge rate and synchrony were calculated to describe SAM responses. There were significant age-related changes in the shape and peak vector strength [best modulation frequency (BMF)] of temporal modulation transfer functions (tMTFs), with no significant age-related changes in rate modulation transfer functions (rMTFs) at BMF. Young neurons exhibited band-pass tMTFs for most SAM conditions while aged fusiform cells exhibited significantly more low-pass or double-peaked tMTFs. There were significant differences in tMTFs between buildup, pauser-buildup, and wide-chopper temporal response types. Young and aged wide-choppers displayed significantly lower vector strength values than the other two temporal DCN response types. Age-related decreases in the number of pauser-buildup response types and increases in wide-chopper types with age reported previously, could account, in part, for the observed loss of temporal coding of the aged fusiform cell. Age-related changes in SAM coding were similar to changes observed with receptor blockade of glycinergic inhibition onto fusiform cells and consistent with previously observed age-related loss of endogenous glycine levels and changes in normal adult glycine receptor function. DCN changes in SAM coding could, in part, underpin temporal processing deficits observed in the elderly. KeywordsDorsal Cochlear Nucleus; Aging; Auditory; Glycine; Amplitude Modulation; Temporal Processing Presbycusis, age-related hearing loss, is a complex disorder that may result in a slow deterioration of peripheral auditory input to auditory regions of the brain (see Willott, 1991; Corresponding Author: Dr. Donald M. Caspary, Department of Pharmacology, Southern Illinois University School of Medicine, P.O. Box 19629, Springfield, IL 62794-9629. Phone: (217) 545-2195, Fax: (217) 545-0145, email: dcaspary@siumed.edu. Publisher's Disclaimer: This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final citable form. Please note that during the production process errors may be discovered which could affect the content, and all legal...

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Divergent response properties of layer-V neurons in rat primary auditory cortex

Cited by 31 publications

References 65 publications

Large-Scale Heterogeneous Representation of Sound Attributes in Rat Primary Auditory Cortex: From Unit Activity to Population Dynamics

Large-Scale Heterogeneous Representation of Sound Attributes in Rat Primary Auditory Cortex: From Unit Activity to Population Dynamics

Inhibitory neurotransmission, plasticity and aging in the mammalian central auditory system

Aged-related loss of temporal processing: Altered responses to amplitude modulated tones in rat dorsal cochlear nucleus

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