scholarly journals Effects of Acetylcholine and Atropine on Plasticity of Central Auditory Neurons Caused by Conditioning in Bats

2001 ◽  
Vol 86 (1) ◽  
pp. 211-225 ◽  
Author(s):  
Weiqing Ji ◽  
Enquan Gao ◽  
Nobuo Suga
Keyword(s):  
Somatosensory Cortex ◽  
Basal Forebrain ◽  
Cortical Neurons ◽  
Frequency Tuning ◽  
Auditory Neurons ◽  
Tuning Curves ◽  
Acoustic Stimuli ◽  
Cholinergic Basal Forebrain ◽  
Big Brown Bat ◽  
Central Auditory Neurons

In the big brown bat ( Eptesicus fuscus), conditioning with acoustic stimuli followed by electric leg-stimulation causes shifts in frequency-tuning curves and best frequencies (hereafter BF shifts) of collicular and cortical neurons, i.e., reorganization of the cochleotopic (frequency) maps in the inferior colliculus (IC) and auditory cortex (AC). The collicular BF shift recovers 180 min after the conditioning, but the cortical BF shift lasts longer than 26 h. The collicular BF shift is not caused by conditioning, as the AC is inactivated during conditioning. Therefore it has been concluded that the collicular BF shift is caused by the corticofugal auditory system. The collicular and cortical BF shifts both are not caused by conditioning as the somatosensory cortex is inactivated during conditioning. Therefore it has been hypothesized that the cortical BF shift is mostly caused by both the subcortical (e.g., collicular) BF shift and the activity of nonauditory systems such as the somatosensory cortex excited by an unconditioned leg-stimulation and the cholinergic basal forebrain. The main aims of our present studies are to examine whether acetylcholine (ACh) applied to the AC augments the collicular and cortical BF shifts caused by the conditioning and whether atropine applied to the AC abolishes the cortical BF shift but not the collicular BF shift, as expected from the preceding hypothesis. In the awake bat, we made the following findings. ACh applied to the AC augments not only the cortical BF shift but also the collicular BF shift through the corticofugal system. Atropine applied to the AC reduces the collicular BF shift and abolishes the cortical BF shift which otherwise would be caused. ACh applied to the IC significantly augments the collicular BF shift but affects the cortical BF shift only slightly. ACh makes the cortical BF shift long-lasting beyond 4 h, but it cannot make the collicular BF shift long-lasting beyond 3 h. Atropine applied to the IC abolishes the collicular BF shift. It reduces the cortical BF shift but does not abolish it. Our findings favor the hypothesis that the BF shifts evoked by the corticofugal system, and an increased ACh level in the AC evoked by the basal forebrain are both necessary to evoke a long-lasting cortical BF shift.

scholarly journals Augmentation of Plasticity of the Central Auditory System by the Basal Forebrain and/or Somatosensory Cortex

2003 ◽  
Vol 89 (1) ◽  
pp. 90-103 ◽  
Author(s):  
Xiaofeng Ma ◽  
Nobuo Suga
Keyword(s):  
Somatosensory Cortex ◽  
Auditory System ◽  
Basal Forebrain ◽  
Cortical Neurons ◽  
Electric Stimulation ◽  
Cortical Plasticity ◽  
Frequency Tuning ◽  
Cortical Stimulation ◽  
Cholinergic Basal Forebrain ◽  
Stimulation Of

Auditory conditioning (associative learning) or focal electric stimulation of the primary auditory cortex (AC) evokes reorganization (plasticity) of the cochleotopic (frequency) map of the inferior colliculus (IC) as well as that of the AC. The reorganization results from shifts in the best frequencies (BFs) and frequency-tuning curves of single neurons. Since the importance of the cholinergic basal forebrain for cortical plasticity and the importance of the somatosensory cortex and the corticofugal auditory system for collicular and cortical plasticity have been demonstrated, Gao and Suga proposed a hypothesis that states that the AC and corticofugal system play an important role in evoking auditory collicular and cortical plasticity and that auditory and somatosensory signals from the cerebral cortex to the basal forebrain play an important role in augmenting collicular and cortical plasticity. To test their hypothesis, we studied whether the amount and the duration of plasticity of both collicular and cortical neurons evoked by electric stimulation of the AC or by acoustic stimulation were increased by electric stimulation of the basal forebrain and/or the somatosensory cortex. In adult big brown bats ( Eptesicus fuscus), we made the following major findings. 1) Collicular and cortical plasticity evoked by electric stimulation of the AC is augmented by electric stimulation of the basal forebrain. The amount of augmentation is larger for cortical plasticity than for collicular plasticity. 2) Collicular and cortical plasticity evoked by AC stimulation is augmented by somatosensory cortical stimulation mimicking fear conditioning. The amount of augmentation is larger for cortical plasticity than for collicular plasticity. 3) Collicular and cortical plasticity evoked by both AC and basal forebrain stimulations is further augmented by somatosensory cortical stimulation. 4) A lesion of the basal forebrain tends to reduce collicular and cortical plasticity evoked by AC stimulation. The reduction is small and statistically insignificant for collicular plasticity but significant for cortical plasticity. 5) The lesion of the basal forebrain eliminates the augmentation of collicular and cortical plasticity that otherwise would be evoked by somatosensory cortical stimulation. 6) Collicular and cortical plasticity evoked by repetitive acoustic stimuli is augmented by basal forebrain and/or somatosensory cortical stimulation. However, the lesion of the basal forebrain eliminates the augmentation of collicular and cortical plasticity that otherwise would be evoked by somatosensory cortical stimulation. These findings support the hypothesis proposed by Gao and Suga.

scholarly journals Sensory experience in Development Balances excitation and Inhibition to stabilize Frequency Tuning in central Auditory neurons

2011 ◽  
Vol 5 ◽  
pp. JEN.S6833
Author(s):  
Kenjiro Seki ◽  
Troy Templeton ◽  
Liisa A. Tremere ◽  
Raphael Pinaud
Keyword(s):  
Receptive Field ◽  
Cortical Neurons ◽  
Frequency Tuning ◽  
Sensory Cues ◽  
Auditory Neurons ◽  
Developmentally Regulated ◽  
Brain Circuits ◽  
New Findings ◽  
Central Auditory Neurons ◽  
Inhibitory Networks

The balance between excitation and inhibition is critical in shaping receptive field tuning properties in sensory neurons and, ultimately, in determining how sensory cues are extracted, transformed and interpreted by brain circuits. New findings suggest that developmentally-regulated, experience-dependent changes in intracortical inhibitory networks are key to defning receptive field tuning properties of auditory cortical neurons.

Anesthesia Changes Frequency Tuning of Neurons in the Rat Primary Auditory Cortex

2001 ◽  
Vol 86 (2) ◽  
pp. 1062-1066 ◽  
Author(s):  
Bernhard H. Gaese ◽  
Joachim Ostwald
Keyword(s):  
Auditory Processing ◽  
Cortical Neurons ◽  
Frequency Tuning ◽  
Primary Auditory Cortex ◽  
Acoustic Stimulation ◽  
Experimental Manipulation ◽  
Central Auditory Processing ◽  
Auditory Neurons ◽  
Response Properties ◽  
Central Auditory Neurons

The vast majority of investigations on central auditory processing so far were conducted under the influence of an anesthetic agent. It remains unclear, however, to what extend even basic response properties of central auditory neurons are influenced by this experimental manipulation. We used a combination of chronic recording in unrestrained animals, computer-controlled randomized acoustic stimulation, and statistical evaluation of responses to directly compare the response characteristics of single neurons in the awake and anesthetized state. Thereby we were able to quantify the effects of pentobarbital/chloral hydrate anesthesia (Equithesin) on rat auditory cortical neurons. During Equithesin anesthesia, only a portion of central neurons were active and some of their basic response properties were changed. Only 29% of the neurons still had a frequency response area. Their tuning sharpness was increased under anesthesia. Most changes are consistent with an enhancement of inhibitory influences during Equithesin anesthesia. Thus when describing response properties of central auditory neurons, the animal's anesthetic state has to be taken into account.

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

2000 ◽  
Vol 83 (4) ◽  
pp. 1856-1863 ◽  
Author(s):  
Syed A. Chowdhury ◽  
Nobuo Suga
Keyword(s):  
Electrical Stimulation ◽  
Auditory Cortex ◽  
Cortical Neurons ◽  
Frequency Tuning ◽  
Acoustic Stimulus ◽  
Primary Auditory Cortex ◽  
Neural Representation ◽  
Tuning Curves ◽  
Big Brown Bat ◽  
Frequency Map

In a search phase of echolocation, big brown bats, Eptesicus fuscus, emit biosonar pulses at a rate of 10/s and listen to echoes. When a short acoustic stimulus was repetitively delivered at this rate, the reorganization of the frequency map of the primary auditory cortex took place at and around the neurons tuned to the frequency of the acoustic stimulus. Such reorganization became larger when the acoustic stimulus was paired with electrical stimulation of the cortical neurons tuned to the frequency of the acoustic stimulus. This reorganization was mainly due to the decrease in the best frequencies of the neurons that had best frequencies slightly higher than those of the electrically stimulated cortical neurons or the frequency of the acoustic stimulus. Neurons with best frequencies slightly lower than those of the acoustically and/or electrically stimulated neurons slightly increased their best frequencies. These changes resulted in the over-representation of repetitively delivered acoustic stimulus. Because the over-representation resulted in under-representation of other frequencies, the changes increased the contrast of the neural representation of the acoustic stimulus. Best frequency shifts for over-representation were associated with sharpening of frequency-tuning curves of 25% of the neurons studied. Because of the increases in both the contrast of neural representation and the sharpness of tuning, the over-representation of the acoustic stimulus is accompanied with an improvement of analysis of the acoustic stimulus.

Noradrenergic Induction of Selective Plasticity in the Frequency Tuning of Auditory Cortex Neurons

2004 ◽  
Vol 92 (3) ◽  
pp. 1445-1463 ◽  
Author(s):  
Yves Manunta ◽  
Jean-Marc Edeline
Keyword(s):  
Auditory Cortex ◽  
Cortical Neurons ◽  
Cortical Plasticity ◽  
Frequency Tuning ◽  
Tone Frequency ◽  
Cortical Cells ◽  
Tuning Curves ◽  
Alpha Receptors ◽  
Frequency Changes ◽  
Selective Effects

Neuromodulators have long been viewed as permissive factors in experience-induced cortical plasticity, both during development and in adulthood. Experiments performed over the last two decades have reported the potency of acetylcholine to promote changes in functional properties of cortical cells in the auditory, visual, and somatosensory modality. In contrast, very few attempts were made with the monoaminergic systems. The present study evaluates how repeated presentation of brief pulses of noradrenaline (NA) concomitant with presentation of a particular tone frequency changes the frequency tuning curves of auditory cortex neurons determined at 20 dB above threshold. After 100 trials of NA-tone pairing, 28% of the cells (19/67) exhibited selective tuning modifications for the frequency paired with NA. All the selective effects were obtained when the paired frequency was within 1/4 of an octave from the initial best frequency. For these cells, selective decreases were prominent (15/19 cases), and these effects lasted ≥15 min after pairing. No selective effects were observed under various control conditions: tone alone ( n = 10 cells), NA alone ( n = 11 cells), pairing with ascorbic acid ( n = 6 cells), or with GABA ( n = 20 cells). Selective effects were observed when the NA-tone pairing was performed in the presence of propranolol (4/10 cells) but not when it was performed in the presence phentolamine (0/13 cells), suggesting that the effects were mediated by alpha receptors. These results indicate that brief increases in noradrenaline concentration can trigger selective modifications in the tuning curves of cortical neurons that, in most of the cases, go in opposite direction compared with those usually reported with acetylcholine.

scholarly journals Tone-Specific and Nonspecific Plasticity of the Auditory Cortex Elicited by Pseudoconditioning: Role of Acetylcholine Receptors and the Somatosensory Cortex

2008 ◽  
Vol 100 (3) ◽  
pp. 1384-1396 ◽  
Author(s):  
Weiqing Ji ◽  
Nobuo Suga
Keyword(s):  
Auditory Cortex ◽  
Receptor Antagonist ◽  
Fear Conditioning ◽  
Somatosensory Cortex ◽  
Acetylcholine Receptors ◽  
Neural Circuit ◽  
Frequency Tuning ◽  
Cholinergic Receptor ◽  
Auditory Neurons ◽  
Specific Change

Experience-dependent plastic changes in the central sensory systems are due to activation of both the sensory and neuromodulatory systems. Nonspecific changes of cortical auditory neurons elicited by pseudoconditioning are quite different from tone-specific changes of the neurons elicited by auditory fear conditioning. Therefore the neural circuit evoking the nonspecific changes must also be different from that evoking the tone-specific changes. We first examined changes in the response properties of cortical auditory neurons of the big brown bat elicited by pseudoconditioning with unpaired tonal (CSu) and electric leg (USu) stimuli and found that it elicited nonspecific changes to CSu (a heart-rate decrease, an auditory response increase, a broadening of frequency tuning, and a decrease in threshold) and, in addition, a small tone-specific change to CSu (a small short-lasting best-frequency shift) only when CSu frequency was 5 kHz lower than the best frequency of a recorded neuron. We then examined the effects of drugs on the cortical changes elicited by the pseudoconditioning. The development of the nonspecific changes was scarcely affected by atropine (a muscarinic cholinergic receptor antagonist) and mecamylamine (a nicotinic cholinergic receptor antagonist) applied to the auditory cortex and by muscimol (a GABAA-receptor agonist) applied to the somatosensory cortex. However, these drugs abolished the small short-lasting tone-specific change as they abolished the large long-lasting tone-specific change elicited by auditory fear conditioning. Our current results indicate that, different from the tone-specific change, the nonspecific changes depend on neither the cholinergic neuromodulator nor the somatosensory cortex.

scholarly journals Influence of Contrast on Orientation and Temporal Frequency Tuning in Ferret Primary Visual Cortex

2004 ◽  
Vol 91 (6) ◽  
pp. 2797-2808 ◽  
Author(s):  
Henry J. Alitto ◽  
W. Martin Usrey
Keyword(s):  
Visual Cortex ◽  
Primary Visual Cortex ◽  
Cortical Neurons ◽  
Frequency Tuning ◽  
Temporal Frequency ◽  
Orientation Tuning ◽  
Visual Response ◽  
Stimulus Contrast ◽  
Tuning Curves ◽  
Simple And Complex Cells

Neurons in primary visual cortex are highly sensitive to the contrast, orientation, and temporal frequency of a visual stimulus. These three stimulus properties can be varied independently of one another, raising the question of how they interact to influence neuronal responses. We recorded from individual neurons in ferret primary visual cortex to determine the influence of stimulus contrast on orientation tuning, temporal-frequency tuning, and latency to visual response. Results show that orientation-tuning bandwidth is not affected by contrast level. Thus neurons in ferret visual cortex display contrast-invariant orientation tuning. Stimulus contrast does, however, influence the structure of orientation-tuning curves as measures of circular variance vary inversely with contrast for both simple and complex cells. This change in circular variance depends, in part, on a contrast-dependent change in the ratio of null to preferred orientation responses. Stimulus contrast also has an influence on the temporal-frequency tuning of cortical neurons. Both simple and complex cells display a contrast-dependent rightward shift in their temporal frequency-tuning curves that results in an increase in the highest temporal frequency needed to produce a half-maximum response (TF50). Results show that the degree of the contrast-dependent increase in TF50 is similar for cortical neurons and neurons in the lateral geniculate nucleus (LGN) and indicate that subcortical mechanisms likely play a major role in establishing the degree of effect displayed by downstream neurons. Finally, results show that LGN and cortical neurons experience a contrast-dependent phase advance in their visual response. This phase advance is most pronounced for cortical neurons indicating a role for both subcortical and cortical mechanisms.

Electrophysiological studies of acetylcholine and the role of the basal forebrain in the somatosensory cortex of the cat. I. Cortical neurons excited by glutamate

1990 ◽  
Vol 64 (4) ◽  
pp. 1199-1211 ◽  
Author(s):  
N. Tremblay ◽  
R. A. Warren ◽  
R. W. Dykes
Keyword(s):  
Somatosensory Cortex ◽  
Basal Forebrain ◽  
Cortical Neurons ◽  
Cholinergic Neurons ◽  
Average Increase ◽  
Average Response ◽  
Electrophysiological Studies ◽  
Release Of Acetylcholine

1. Microelectrodes attached to iontophoretic pipettes were used to isolate 410 single neurons in the primary somatosensory cortex of halothane-anesthetized cats. Basal forebrain (BF) stimulation, when paired with pulses of iontophoretically administered glutamate, affected the responsiveness in 24 (54%) of 39 neurons; 17 were facilitated, and seven were inhibited. Five minutes after BF stimulation the average response for a sample of 20 cells was enhanced by 45% (+/- 19). All but one of the effects lasted as long as the cell was studied, often greater than 1 h. 2. When atropine was administered while the BF was stimulated during glutamate excitation, 7 of 16 cells were enhanced, but the average increase was only 16% (+/- 15) for a sample of 15 cells. After the atropine had dissipated, four cells were enhanced by the BF stimulus. In three of these the enhancement had been blocked previously by atropine. 3. BF stimulation had effects similar to iontophoretically administered acetylcholine (ACh), but the effects appeared more frequently with BF stimulation than they had with acetylcholine administration. 4. We propose that the enhanced neuronal responsiveness is due to the release of acetylcholine by cortical terminals of cholinergic neurons located in the BF. The BF stimulus may be more effective than acetylcholine administration because corticopetal cholinergic fibers may end in the immediate vicinity of receptors responsible for long-term changes in membrane permeability.

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