Lateral Inhibition for Center-Surround Reorganization of the Frequency Map of Bat Auditory Cortex

Ma, Xiaofeng; Suga, Nobuo

doi:10.1152/jn.00301.2004

Cited by 33 publications

(25 citation statements)

References 38 publications

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“…As shown in the present paper, electric stimulation accompanied with ACh applied to the AC evoked the long-term plastic change (BF shift) in the AC, as auditory fear conditioning does. This finding and others (3,4,11,12) indicate that the short-term cortical BF shift is evoked by the neural circuit intrinsic to the AC and corticofugal feedback system and is augmented by the cholinergic basal forebrain, as hypothesized by Gao and Suga (2). However, there are several intriguing problems to be solved.…”

Section: Discussionsupporting

confidence: 65%

“…3-5. Focal electric stimulation of the AC (ES a ) evokes BF shifts of cortical and collicular neurons (9,(22)(23)(24)(25). ACh applied to the AC without conditioning or cortical electric stimulation evokes neither cortical nor collicular BF shifts, but it augments BF shifts evoked by conditioning (4) or cortical electric stimulation (12). In Fig.…”

Section: Resultsmentioning

confidence: 96%

“…The direction of the cortical and collicular BF shifts evoked by focal electric stimulation of the auditory cortex (AC) changes when an antagonist, bicuculline (11,12), or an agonist, muscimol (12), of GABA A receptors is applied to the AC. This finding indicates that the neural circuit within the AC plays an important role in evoking the BF shifts.…”

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confidence: 99%

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Long-term cortical plasticity evoked by electric stimulation and acetylcholine applied to the auditory cortex

Suga²

2005

Proc. Natl. Acad. Sci. U.S.A.

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Auditory fear conditioning with tone bursts followed by electric leg stimulation activates neurons not only in the auditory and somatosensory systems but also in many other regions of the brain and elicits shifts in the best frequencies (BFs) of collicular and cortical neurons, i.e., reorganization of the frequency (cochleotopic) maps in the inferior colliculus and auditory cortex (AC). What are the neural elements minimally necessary for evoking long-term cortical BF shifts? We found that: (i) both electric stimulation and acetylcholine applied to the AC evoke the long-term cortical BF shift as does the conditioning; (ii) both electric stimulation of the AC and acetylcholine applied to the inferior colliculus increase the short-term collicular BF shift evoked by the cortical electric stimulation but do not change it into long-term; and (iii) as this short-term collicular BF shift is blocked by atropine, the development of the long-term cortical BF shift becomes slow and small. Therefore, the most essential neural elements for evoking the long-term cortical BF shift are the AC, corticofugal feedback and the cholinergic nucleus. Our current data support the GaoSuga model, which hypothesizes that the small short-term cortical BF shifts are evoked by tonal stimuli without the association of conditioned and unconditioned stimuli in the multisensory thalamic nuclei and that these BF shifts are augmented and changed into the large long-term BF shifts by cholinergic neurons.bat ͉ best frequency ͉ conditioning ͉ corticofungal modulation ͉ frequency tuning L arge long-term cortical best frequency (BF) shifts can be evoked by either auditory fear conditioning (1-5) or tone bursts paired with electric stimulation of the cholinergic basal forebrain (6-9). Tone bursts used as a conditioned stimulus (CS) activate neurons in the ascending and descending auditory systems, association cortex, multisensory subcortical nuclei, amygdala, and modulatory systems such as the cholinergic basal forebrain, etc. Electric leg (or foot) stimulation used as an unconditioned stimulus (US) activates neurons in the ascending and descending somatosensory systems and in other brain regions, as do the tone bursts. Electric stimulation of the cholinergic basal forebrain activates neurons not only in the cholinergic basal forebrain but also in the cerebral cortex, and amygdala, etc. (10). What are the neural elements minimally necessary to evoke the large long-term cortical BF shift?There have been five major neurophysiological findings directly related to the cortical and collicular BF shifts.1. The direction of the cortical and collicular BF shifts evoked by focal electric stimulation of the auditory cortex (AC) changes when an antagonist, bicuculline (11, 12), or an agonist, muscimol (12), of GABA A receptors is applied to the AC. This finding indicates that the neural circuit within the AC plays an important role in evoking the BF shifts. 2. Inactivation of the somatosensory cortex by muscimol does not affect cortical auditory responses but sele...

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Section: Discussionsupporting

confidence: 65%

Section: Resultsmentioning

confidence: 96%

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Long-term cortical plasticity evoked by electric stimulation and acetylcholine applied to the auditory cortex

Suga²

2005

Proc. Natl. Acad. Sci. U.S.A.

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“…However, we may speculate the mechanism for the serotonergic modulation. The direction of the BF shift depends on the balance between excitation and inhibition occurring in the AI, because muscimol (an agonist of GABA A receptors) changes the centripetal BF shift into a centrifugal BF shift (Ma and Suga, 2004), and bicucullin (an antagonist of GABA A receptors) changes the centrifugal BF shift into a centripetal BF shift (Xiao and Suga, 2002;Ma and Suga, 2004). Ritanserin (a 5-HT 2A receptor antagonist) suppressed the cortical auditory response and changed the centripetal BF shift into a centrifugal BF shift.…”

Section: Discussionmentioning

confidence: 99%

Serotonergic Modulation of Plasticity of the Auditory Cortex Elicited by Fear Conditioning

Suga²

2007

J. Neurosci.

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In the awake big brown bat, 30 min auditory fear conditioning elicits conditioned heart rate decrease and long-term best frequency (BF) shifts of cortical auditory neurons toward the frequency of the conditioned tone; 15 min conditioning elicits subthreshold cortical BF shifts that can be augmented by acetylcholine. The fear conditioning causes stress and an increase in the cortical serotonin (5-HT) level. Serotonergic neurons in the raphe nuclei associated with stress and fear project to the cerebral cortex and cholinergic basal forebrain. Recently, it has been shown that 5-HT 2A receptors are mostly expressed on pyramidal neurons and their activation improves learning and memory. We applied 5-HT, an agonist (␣-methyl-5-HT), or an antagonist (ritanserin) of 5-HT 2A receptors to the primary auditory cortex and discovered the following drug effects: (1) 5-HT had no effect on the conditioned heart rate change, although it reduced the auditory responses; (2) 4 mM 5-HT augmented the subthreshold BF shifts, whereas 20 mM 5-HT did not; (3) 20 mM 5-HT reduced the long-term BF shifts and changed them into short-term; (4) ␣-methyl-5-HT increased the auditory responses and augmented the subthreshold BF shifts as well as the long-term BF shifts; (5) in contrast, ritanserin reduced the auditory responses and reversed the direction of the BF shifts. Our data indicate that the BF shift can be modulated by serotonergic neurons that augment or reduce the BF shift or even reverse the direction of the BF shift. Therefore, not only the cholinergic system, but also the serotonergic system, plays an important role in cortical plasticity according to behavioral demands.

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“…It has been demonstrated that pyramidal cell tuning in the visual and auditory systems depends on a balance of thalamocortical excitatory inputs and local circuit inhibition (Wehr and Zador, 2003;Ma and Suga, 2004). For example, in the visual cortex (V1), narrow orientation tuning is generated by both an enhancement near the preferred orientation caused by specific inputs from the LGN and corticocortical amplification, and by global suppression supplied by cortical inhibition (Ferster and Miller, 2000;Shapley et al, 2003).…”

Section: Introductionmentioning

confidence: 99%

Dynamic Sculpting of Directional Tuning in the Primate Motor Cortex during Three-Dimensional Reaching

Merchant¹,

Naselaris

Georgopoulos³

2008

J. Neurosci.

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In the present study, we investigated how directional tuning of putative pyramidal cells is sharpened by inhibition from neighboring interneurons. First, different functional and electrophysiological criteria were used to identify putative pyramidal and interneuronal subtypes in a large database of motor cortical cells recorded during performance of the three-dimensional center-out task. Then we analyzed the relationship between the magnitude of inhibition and the tuning width, and a significant decrease of the latter as a function of the former was found in a population of putative pyramidal cells. In fact, the coupling of inhibition with narrow tuning was observed before and during movement execution on a cell-by-cell basis, indicating an important dynamic role of inhibition during movement control. Overall, these results suggest that local inhibition is involved in sculpting the directional specificity of a group of putative pyramidal neurons in the motor cortex.

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Lateral Inhibition for Center-Surround Reorganization of the Frequency Map of Bat Auditory Cortex

Cited by 33 publications

References 38 publications

Long-term cortical plasticity evoked by electric stimulation and acetylcholine applied to the auditory cortex

Long-term cortical plasticity evoked by electric stimulation and acetylcholine applied to the auditory cortex

Serotonergic Modulation of Plasticity of the Auditory Cortex Elicited by Fear Conditioning

Dynamic Sculpting of Directional Tuning in the Primate Motor Cortex during Three-Dimensional Reaching

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