Tone-Evoked Excitatory and Inhibitory Synaptic Conductances of Primary Auditory Cortex Neurons

Tan, Andrew Y. Y.; Zhang, Li I.; Merzenich, Michael M.; Schreiner, Christoph E.

doi:10.1152/jn.01020.2003

Cited by 249 publications

(275 citation statements)

References 64 publications

(43 reference statements)

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“…Membrane potential dynamics in the auditory cortex of intact animals have been examined previously by several groups (De Ribaupierre et al, 1972;Volkov and Galazyuk 1992;Ojima and Murakami, 2002;Wehr and Zador, 2003;Zhang et al, 2003;DeWeese and Zador, 2004;Tan et al, 2004;Las et al, 2005), and the present data appear consistent with that body of work. In particular, examples of subthreshold activity presented in those reports typically appeared to consist of brief excursions from rest, similar to the bumps that dominate the dynamics we observed.…”

Section: Discussionsupporting

confidence: 90%

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Non-Gaussian Membrane Potential Dynamics Imply Sparse, Synchronous Activity in Auditory Cortex

DeWeese¹,

Zador²

2006

J. Neurosci.

148

134

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Many models of cortical dynamics have focused on the high-firing regime, in which neurons are driven near their maximal rate. Here we consider the responses of neurons in auditory cortex under typical low-firing rate conditions, when stimuli have not been optimized to drive neurons maximally. We used whole-cell patch-clamp recording in vivo to measure subthreshold membrane potential fluctuations in rat primary auditory cortex in both the anesthetized and awake preparations. By analyzing the subthreshold membrane potential dynamics on single trials, we made inferences about the underlying population activity. We found that, during both spontaneous and evoked responses, membrane potential was highly non-Gaussian, with dynamics consisting of occasional large excursions (sometimes tens of millivolts), much larger than the small fluctuations predicted by most random walk models that predict a Gaussian distribution of membrane potential. Thus, presynaptic inputs under these conditions are organized into quiescent periods punctuated by brief highly synchronous volleys, or "bumps." These bumps were typically so brief that they could not be well characterized as "up states" or "down states." We estimate that hundreds, perhaps thousands, of presynaptic neurons participate in the largest volleys. These dynamics suggest a computational scheme in which spike timing is controlled by concerted firing among input neurons rather than by small fluctuations in a sea of background activity.

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Section: Discussionsupporting

confidence: 90%

“…As expected from previous results Zhang et al, 2003;DeWeese and Zador, 2004;Tan et al, 2004;Las et al, 2005), tone-evoked responses were brief and often occurred with a short latency immediately after the tone (Figs. 2a1, 3a).…”

Section: Subthreshold Recordings In Auditory Cortexsupporting

confidence: 89%

Non-Gaussian Membrane Potential Dynamics Imply Sparse, Synchronous Activity in Auditory Cortex

DeWeese¹,

Zador²

2006

J. Neurosci.

148

134

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“…Cortical cells can be reasonably clamped before and after cocktail application with clamping deviation within around ± 5 mV(see Supplementary Information Part 2). For a few cases when both excitatory and inhibitory TRFs were obtained before cortical silencing, we derived the excitatory synaptic conductance Ge(t) [25][26][27]29,33,41,42 according to I(t, V) = Gr(V−Er) + Ge(t)(V−Ee) + Gi(t)(V−Ei), where V is the clamping voltage, Gr is the resting conductance, Er is the resting potential; Ee and Ei are the reversal potentials for excitatory and inhibitory synaptic currents, respectively; and I(t, V) is the current amplitude under V, and V (t) is given by V(t) = Vc − Rs*I(t), where Rs was the effective series resistance and Vc is the clamping voltage applied. The liquid junction potential is estimated to be 12 mV.…”

Section: In Vivo Whole-cell Recordingmentioning

confidence: 99%

Defining cortical frequency tuning with recurrent excitatory circuitry

et al. 2007

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Neurons in the recipient layers of sensory cortices receive excitatory input of two major sources: the feedforward thalamocortical and recurrent intracortical inputs. To address their respective functional roles, we developed a novel method to silence cortex by activating GABA A while blocking GABA B receptors. In the rat primary auditory cortex, in vivo whole-cell recording from the same neuron before and after local cortical silencing revealed that thalamic input occupies the same area of frequency-intensity tonal receptive field as the total excitatory input, but exhibits a flattened tuning curve. In contrast, excitatory intracortical input is sharply tuned, with a tuning curve closely matching that of suprathreshold responses. This can be attributed to a selective amplification of cortical cells' responses at preferred frequencies by intracortical inputs from similarly tuned neurons. Thus, weaklytuned thalamocortical inputs determine the subthreshold responding range, while intracortical inputs largely define the tuning. Such circuits may ensure a faithful conveyance of sensory information.Although many aspects of representation/processing function of neurons in the recipient layers of cortex appear to reflect converging thalamocortical inputs 1-5 , the functional role and the underlying pattern of thalamocortical and, in particular, intracortical excitatory inputs remain unsolved 6-9 . Extensive efforts have been made to understand the thalamocortical contribution to cortical responses. These previous studies can be mostly categorized into two types: 1) directly compare the response properties between simultaneously recorded neurons in the thalamus and cortex 1,10-12 ; and 2) isolate thalamocortical input by preventing spiking of cortical neurons 2,13-17 . The first type of studies mostly used extracellular recordings, and identified putatively connected thalamic and cortical units based on temporal correlation between their spikes. This approach provides information on the tuning properties of individual thalamic and cortical neurons as well as the nature of connection between them. A recent study in the somatosensory cortex 5 , by pairing extracellular recording of thalamic neurons with intracellular recording of cortical cells, suggests that cortical neurons receive a number of weak but synchronously activated thalamic inputs, which exhibit similar tuning properties as the recorded cortical neuron. However, since the pattern underlying divergent output connections made by a single thalamic neuron, or convergent thalamic inputs made on a single cortical

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“…However, these early studies did not systematically explore the relationship between frequency and level tuning, leaving open the possibility that nonmonotonic rate-level tuning is limited to frequencies at or near the best frequency (BF) of a unit. In the ϳ25 years since these studies, however, many studies have described FRAs of primary auditory cortex (A1) neurons as level intolerant in a variety of species such as cats (Calford et al, 1983;Heil et al, 1992;Schreiner et al, 2000;Moshitch et al, 2006), rats (Kilgard and Merzenich, 1999;Tan et al, 2004), mice (Linden et al, 2003), ferrets (Shamma et al, 1993), and macaque monkeys (Recanzone et al, 2000), to name a few. Except for the study by Recanzone et al (2000), the above cited studies were all conducted in anesthetized animals.…”

Section: Introductionmentioning

confidence: 99%

Level Invariant Representation of Sounds by Populations of Neurons in Primary Auditory Cortex

Sadagopan

Wang²

2008

J. Neurosci.

136

168

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A fundamental feature of auditory perception is the constancy of sound recognition over a large range of intensities. Although this invariance has been described in behavioral studies, the underlying neural mechanism is essentially unknown. Here we show a putative level-invariant representation of sounds by populations of neurons in primary auditory cortex (A1) that may provide a neural basis for the behavioral observations. Previous studies reported that pure-tone frequency tuning of most A1 neurons widens with increasing sound level. In sharp contrast, we found that a large proportion of neurons in A1 of awake marmosets were narrowly and separably tuned to both frequency and sound level. Tuning characteristics and firing rates of the neural population were preserved across all tested sound levels. These response properties lead to a level-invariant representation of sounds over the population of A1 neurons. Such a representation is an important step for robust feature recognition in natural environments.

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Tone-Evoked Excitatory and Inhibitory Synaptic Conductances of Primary Auditory Cortex Neurons

Cited by 249 publications

References 64 publications

Non-Gaussian Membrane Potential Dynamics Imply Sparse, Synchronous Activity in Auditory Cortex

Non-Gaussian Membrane Potential Dynamics Imply Sparse, Synchronous Activity in Auditory Cortex

Defining cortical frequency tuning with recurrent excitatory circuitry

Level Invariant Representation of Sounds by Populations of Neurons in Primary Auditory Cortex

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