Reorganization of the Frequency Map of the Auditory Cortex Evoked by Cortical Electrical Stimulation in the Big Brown Bat

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Auditory conditioning (associative learning) causes reorganization of the cochleotopic (frequency) maps of the primary auditory cortex (AI) and the inferior colliculus. Focal electric stimulation of the AI also evokes basically the same cortical and collicular reorganization as that caused by conditioning. Therefore, part of the neural mechanism for the plasticity of the central auditory system caused by conditioning can be explored by focal electric stimulation of the AI. The reorganization is due to shifts in best frequencies (BFs) together with shifts in frequency-tuning curves of single neurons. In the AI of the Mongolian gerbil (Meriones unguiculatus) and the posterior division of the AI of the mustached bat (Pteronotus parnellii), focal electric stimulation evokes BF shifts of cortical auditory neurons located within a 0.7-mm distance along the frequency axis. The amount and direction of BF shift differ depending on the relationship in BF between stimulated and recorded neurons, and between the gerbil and mustached bat. Comparison in BF shift between different mammalian species and between different cortical areas of a single species indicates that BF shift toward the BF of electrically stimulated cortical neurons (centripetal BF shift) is common in the AI, whereas BF shift away from the BF of electrically stimulated cortical neurons (centrifugal BF shift) is special. Therefore, we propose a hypothesis that reorganization, and accordingly organization, of cortical auditory areas caused by associative learning can be quite different between specialized and nonspecialized (ordinary) areas of the auditory cortex.bat ͉ gerbil ͉ hearing ͉ reorganization of cortex ͉ tonotopic map I n the big brown bat (Eptesicus fuscus), auditory responses, frequency-tuning curves, best frequencies (BFs), and the frequency (cochleotopic) map in the inferior colliculus (IC) change according to acoustic signals frequently heard by the animal (1, 2) and also by auditory conditioning, i.e., associative learning (2, 3). Inactivation of the primary auditory cortex (AI) during the conditioning abolishes these collicular changes. Therefore, the corticofugal (descending) auditory system plays an essential role in the plasticity of the IC (2, 3). The conditioning evokes not only collicular changes, but also changes in the AI. Cortical changes are almost the same as collicular changes in amount but different in time course (3). Focal electric stimulation of the AI also evokes the same changes in the IC (1, 4) and AI (4, 5) as those evoked by repetitive acoustic stimuli or auditory conditioning. The cortical and collicular changes evoked by the electric stimulation are augmented by electric stimulation of the cholinergic basal forebrain (4) or by acetylcholine applied to the AI, as expected (6). These findings indicate that BF shifts evoked by focal electric stimulation are directly related to a normal function: reorganization of the central auditory system caused by associative learning. Therefore, the mechanism for plasticity of the audit...

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Plasticity of the cochleotopic (frequency) map in specialized and nonspecialized auditory cortices

Sakai

Suga

2001

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“…These two types of BF shifts occur in a specific spatial pattern along the frequency axis in the auditory cortex (AC), medial geniculate body, and inferior colliculus. The spatial pattern is basically the same in the AC and the inferior colliculus of the big brown bat (3,5,6,9) and the mustached bat (1,2,10). In the ACs of the big brown bat (5,6) and Mongolian gerbil (8), centripetal BF shifts occur in a large area surrounding the matched neurons, and small centrifugal BF shifts occur in the narrow zone surrounding this large centripetal area; i.e., center-surround reorganization occurs.…”

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confidence: 97%

“…The shift of a BF, together with a frequency-tuning curve, is called a BF shift. Such corticofugal modulation, called egocentric selection (1), improves the input to the stimulated cortical neurons and the subcortical and cortical representations of the stimulus parameters to which the stimulated cortical neurons are tuned (2)(3)(4)(5)(6)(7)(8) There are two types of BF shifts: centripetal and centrifugal. Centripetal BF shifts are the shifts toward the BF of electrically stimulated cortical neurons, and centrifugal BF shifts are the shifts away from the stimulated cortical BF.…”

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Reorganization of the auditory cortex specialized for echo-delay processing in the mustached bat

Xiao¹,

Suga²

2004

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Focal excess sensory stimulation evokes reorganization of a sensory system. It is usually an expansion of the neural representation of that stimulus resulting from the shifts of the tuning curves (receptive fields) of neurons toward those of the stimulated neurons. The auditory cortex of the mustached bat has an area that is highly specialized for the processing of target-distance information carried by echo delays. In this area, however, reorganization is due to shifts of the delay-tuning curves of neurons away from those of the stimulated cortical neurons. Elimination of inhibition in the target-distance processing area in the auditory cortex by a drug reverses the direction of the shifts in neural tuning curves. Therefore, such unique reorganization in the time domain is due to strong lateral inhibition in the highly specialized area of the auditory cortex.bicuculline ͉ centrifugal shift ͉ centripetal shift ͉ delay tuning ͉ plasticity E lectric stimulation of cortical auditory neurons evokes both facilitation and inhibition of the auditory responses of cortical and subcortical neurons. The amount of facilitation and inhibition varies with the frequency of a tone burst to which the neurons respond and with the relationship in frequency tuning between the stimulated and recorded neurons. When the best frequency (BF) of a recorded neuron matches that of a stimulated cortical neuron, the response of the matched neuron to its BF is often augmented, and the responses at frequencies lower and͞or higher than the BF are inhibited. When unmatched, the response of the unmatched neuron is inhibited at its BF and is facilitated at non-BFs. As a result, frequency tuning of the unmatched neuron is shifted. The shift of a BF, together with a frequency-tuning curve, is called a BF shift. Such corticofugal modulation, called egocentric selection (1), improves the input to the stimulated cortical neurons and the subcortical and cortical representations of the stimulus parameters to which the stimulated cortical neurons are tuned (2)(3)(4)(5)(6)(7)(8) There are two types of BF shifts: centripetal and centrifugal. Centripetal BF shifts are the shifts toward the BF of electrically stimulated cortical neurons, and centrifugal BF shifts are the shifts away from the stimulated cortical BF. These two types of BF shifts occur in a specific spatial pattern along the frequency axis in the auditory cortex (AC), medial geniculate body, and inferior colliculus. The spatial pattern is basically the same in the AC and the inferior colliculus of the big brown bat (3,5,6,9) and the mustached bat (1, 2, 10). In the ACs of the big brown bat (5, 6) and Mongolian gerbil (8), centripetal BF shifts occur in a large area surrounding the matched neurons, and small centrifugal BF shifts occur in the narrow zone surrounding this large centripetal area; i.e., center-surround reorganization occurs. Because centrifugal BF shifts are small, the major reorganization in these ACs is due to centripetal BF shifts. In the Doppler-shifted constant frequency (DSCF)...

“…The number of neurons studied for a given ACh or atropine application is shown by a number at the end of each curve in Figs. 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).…”

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confidence: 99%

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

Suga²

2005

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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...