scholarly journals Corticofugal Feedback for Collicular Plasticity Evoked by Electric Stimulation of the Inferior Colliculus

2005 ◽  
Vol 94 (4) ◽  
pp. 2676-2682 ◽  
Author(s):  
Yongkui Zhang ◽  
Nobuo Suga

Focal electric stimulation of the auditory cortex, 30-min repetitive acoustic stimulation, and auditory fear conditioning each evoke shifts of the frequency-tuning curves [hereafter, best frequency (BF) shifts] of cortical and collicular neurons. The short-term collicular BF shift is produced by the corticofugal system and primarily depends on the relationship in BF between a recorded collicular and a stimulated cortical neuron or between the BF of a recorded collicular neuron and the frequency of an acoustic stimulus. However, it has been unknown whether focal electric stimulation of the inferior colliculus evokes the collicular BF shift and whether the collicular BF shift, if evoked, depends on corticofugal feedback. In our present research with the awake big brown bat, we found that focal electric stimulation of collicular neurons evoked the BF shifts of collicular neurons located near the stimulated ones; that there were two types of BF shifts: centripetal and centrifugal BF shifts, i.e., shifts toward and shifts away from the BF of stimulated neurons, respectively; and that the development of these collicular BF shifts was blocked by inactivation of the auditory cortex. Our data indicate that the collicular BF shifts (plasticity) evoked by collicular electric stimulation depended on corticofugal feedback. It should be noted that collicular BF shifts also depend on acetylcholine because it has been demonstrated that atropine (an antagonist of muscarinic acetylcholine receptors) applied to the IC blocks the development of collicular BF shifts.

2003 ◽  
Vol 90 (3) ◽  
pp. 1904-1909 ◽  
Author(s):  
Weiqing Ji ◽  
Nobuo Suga

Reorganization of the frequency map in the central auditory system is based on shifts in the best frequencies (BFs; hereafter, BF shifts), together with the frequency-response curves, of auditory neurons. In the big brown bat, conditioning with acoustic stimulation followed by electric leg-stimulation causes BF shifts of collicular and cortical neurons. The collicular BF shift develops quickly and is short term, whereas the cortical BF shift develops slowly and is long term. The acetycholine level in the auditory cortex must be high during conditioning to develop these BF shifts. We studied the effect of atropine (an antagonist of muscarinic acetylcholine receptors) applied to the auditory cortex on the development of the long-term cortical BF shift in the awake bat caused by a 30-min conditioning session. We found 1) the cortical BF shift starts to develop ∼15 min after the onset of the conditioning, gradually increases over 60 min, and reaches a plateau, 2) the cortical BF shift changes from short to long term ∼45 min after the onset of the conditioning, 3) the cortical BF shift can plateau at different frequencies between the BF of a given neuron in the control condition and the frequency of the conditioning tone, 4) the maximum BF shift is determined ∼70 min after the onset of the conditioning, and 5) acetylcholine plays an important role in the development of the cortical BF shift. Its role ends ∼180 min after the onset of the conditioning.


2004 ◽  
Vol 92 (6) ◽  
pp. 3192-3199 ◽  
Author(s):  
Xiaofeng Ma ◽  
Nobuo Suga

Repetitive acoustic stimulation, auditory fear conditioning, and focal electric stimulation of the auditory cortex (AC) each evoke the reorganization of the central auditory system. Our current study of the big brown bat indicates that focal electric stimulation of the AC evokes center-surround reorganization of the frequency map of the AC. In the center, the neuron's best frequencies (BFs), together with their frequency–tuning curves, shift toward the BFs of electrically stimulated cortical neurons (centripetal BF shifts). In the surround, BFs shift away from the stimulated cortical BF (centrifugal BF shifts). Centripetal BF shifts are much larger than centrifugal BF shifts. An antagonist (bicuculline methiodide) of inhibitory synaptic transmitter receptors changes centrifugal BF shifts into centripetal BF shifts, whereas its agonist (muscimol) changes centripetal BF shifts into centrifugal BF shifts. This reorganization of the AC thus depends on a balance between facilitation and inhibition evoked by focal cortical electric stimulation. Unlike neurons in the AC of the big brown bat, neurons in the Doppler-shifted constant-frequency (DSCF) area of the AC of the mustached bat are highly specialized for fine-frequency analysis and show almost exclusively centrifugal BF shifts for focal electric stimulation of the DSCF area. Our current data indicate that in the highly specialized area, lateral inhibition is strong compared with the less-specialized area and that the specialized and nonspecialized areas both share the same inhibitory mechanism for centrifugal BF shifts.


2008 ◽  
Vol 99 (5) ◽  
pp. 2347-2356 ◽  
Author(s):  
Kyle T. Nakamoto ◽  
Simon J. Jones ◽  
Alan R. Palmer

The function of the profuse descending innervation from the auditory cortex is largely unknown; however, recent studies have demonstrated that focal stimulation of auditory cortex effects frequency tuning curves, duration tuning, and other auditory parameters in the inferior colliculus. Here we demonstrate that, in an anesthetized guinea pig, nonfocal deactivation of the auditory cortex alters the sensitivity of populations of neurons in the inferior colliculus (IC) to one of the major cues for the localization of sound in space, interaural level differences (ILDs). Primary and secondary auditory cortical areas were inactivated by cooling. The ILD functions of 46% of IC cells changed when the cortex was inactivated. In extreme cases, the ILD functions changed from monotonic to nonmonotonic during cooling and vice versa. Eight percent of the cells became unresponsive after deactivation of the auditory cortex. Deactivation of the cortex has previously been shown to alter the maximum spike count of cells in the IC; the change in normalized ILD functions is shown to be separate from this effect. In some cases, the ILD function changed shape when there was no change in the maximum spike count and in other cases there was no change in the shape of the ILD function even though there was a large change in the maximum spike count. Overall, the sensitivity of the IC neural population to ILD is radically altered by the corticofugal pathway.


2012 ◽  
Vol 108 (3) ◽  
pp. 935-942 ◽  
Author(s):  
Jie Tang ◽  
Weiguo Yang ◽  
Nobuo Suga

The central auditory system consists of the lemniscal and nonlemniscal pathways or systems, which are anatomically and physiologically different from each other. In the thalamus, the ventral division of the medial geniculate body (MGBv) belongs to the lemniscal system, whereas its medial (MGBm) and dorsal (MGBd) divisions belong to the nonlemniscal system. Lemniscal neurons are sharply frequency-tuned and provide highly frequency-specific information to the primary auditory cortex (AI), whereas nonlemniscal neurons are generally broadly frequency-tuned and project widely to cortical auditory areas including AI. These two systems are presumably different not only in auditory signal processing, but also in eliciting cortical plastic changes. Electric stimulation of narrowly frequency-tuned MGBv neurons evokes the shift of the frequency-tuning curves of AI neurons toward the tuning curves of the stimulated MGBv neurons (tone-specific plasticity). In contrast, electric stimulation of broadly frequency-tuned MGBm neurons augments the auditory responses of AI neurons and broadens their frequency-tuning curves (nonspecific plasticity). In our current studies, we found that electric stimulation of AI evoked tone-specific plastic changes of the MGBv neurons, whereas it degraded the frequency tuning of MGBm neurons by inhibiting their auditory responses. AI apparently modulates the lemniscal and nonlemniscal thalamic neurons in quite different ways. High MGBm activity presumably makes AI neurons less favorable for fine auditory signal processing, whereas high MGBv activity makes AI neurons more suitable for fine processing of specific auditory signals and reduces MGBm activity.


2008 ◽  
Vol 100 (3) ◽  
pp. 1384-1396 ◽  
Author(s):  
Weiqing Ji ◽  
Nobuo Suga

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.


2001 ◽  
Vol 85 (3) ◽  
pp. 1078-1087 ◽  
Author(s):  
Xiaofeng Ma ◽  
Nobuo Suga

Recent findings indicate that the corticofugal system would play an important role in cortical plasticity as well as collicular plasticity. To understand the role of the corticofugal system in plasticity, therefore, we studied the amount and the time course of plasticity in the inferior colliculus (IC) and auditory cortex (AC) evoked by focal electrical stimulation of the AC and also the effect of electrical stimulation of the somatosensory cortex on the plasticity evoked by the stimulation of the AC. In adult big brown bats ( Eptesicus fuscus), we made the following major findings. 1) Electric stimulation of the AC evokes best frequency (BF) shifts, i.e., shifts in frequency-response curves of collicular and cortical neurons. These BF shifts start to occur within 2 min, reach a maximum (or plateau) at 30 min, and then recover ∼180 min after a 30-min-long stimulus session. When the stimulus session is lengthened from 30 to 90 min, the plateau lasts ∼60 min, but BF shifts recover ∼180 min after the session. 2) The electric stimulation of the somatosensory cortex delivered immediately after that of the AC, as in fear conditioning, evokes a dramatic lengthening of the recovery period of the cortical BF shifts but not that of the collicular BF shift. The electric stimulation of the somatosensory cortex delivered before that of the AC, as in backward conditioning, has no effect on the collicular and cortical BF shifts. 3) Electric stimulation of the AC evokes BF shifts not only in the ipsilateral IC and AC but also in the contralateral IC and AC. BF shifts are smaller in amount and shorter in recovery time for contralateral collicular and cortical neurons than for ipsilateral ones. Our findings support the hypothesis that the AC and the corticofugal system have an intrinsic mechanism for reorganization of the IC and AC, that the reorganization is highly specific to a value of an acoustic parameter (frequency), and that the reorganization is augmented by excitation of nonauditory sensory cortex that makes the acoustic stimulus behaviorally relevant to the animal through associative learning.


1973 ◽  
Vol 38 (3) ◽  
pp. 320-325 ◽  
Author(s):  
Ronald R. Tasker ◽  
L. W. Organ

✓ Auditory hallucinations were produced by electrical stimulation of the human upper brain stem during stereotaxic operations. The responses were confined to stimulation of the inferior colliculus, brachium of the inferior colliculus, medial geniculate body, and auditory radiations. Anatomical confirmation of an auditory site was obtained in one patient. The hallucination produced was a low-pitched nonspecific auditory “paresthesia” independent of the structure stimulated, the conditions of stimulation, or sonotopic factors. The effect was identical to that reported from stimulating the primary auditory cortex, and virtually all responses were contralateral. These observations have led to the following generalizations concerning electrical stimulation of the somesthetic, auditory, vestibular, and visual pathways within the human brain stem: the hallucination induced in each is the response to comparable conditions of stimulation, is nonspecific, independent of stimulation site, confined to the primary pathway concerned, chiefly contralateral, and identical to that induced by stimulating the corresponding primary auditory cortex. No sensory responses are found in the brain stem corresponding to those from the sensory association cortex.


2008 ◽  
Vol 100 (2) ◽  
pp. 1127-1134 ◽  
Author(s):  
Xiaofeng Ma ◽  
Nobuo Suga

The central auditory system creates various types of neurons tuned to different acoustic parameters other than a specific frequency. The response latency of auditory neurons typically shortens with an increase in stimulus intensity. However, ∼10% of collicular neurons of the little brown bat show a “paradoxical latency-shift (PLS)”: long latencies to intense sounds but short latencies to weak sounds. These neurons presumably are involved in the processing of target distance information carried by a pair of an intense biosonar pulse and its weak echo. Our current studies show that collicular PLS neurons of the big brown bat are modulated by the corticofugal (descending) system. Electric stimulation of cortical auditory neurons evoked two types of changes in the PLS neurons, depending on the relationship in the best frequency (BF) between the stimulated cortical and recorded collicular neurons. When the BF was matched between them, the cortical stimulation did not shift the BFs of the collicular neurons and shortened their response latencies at intense sounds so that the PLS became smaller. When the BF was unmatched, however, the cortical stimulation shifted the BFs of the collicular neurons and lengthened their response latencies at intense sounds, so that the PLS became larger. Cortical electric stimulation also modulated the response latencies of non-PLS neurons. It produced an inhibitory frequency tuning curve or curves. Our findings indicate that corticofugal feedback is involved in shaping the spectrotemporal patterns of responses of subcortical auditory neurons presumably through inhibition.


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