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

Abstract

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...

Specific auditory memory induced by nucleus basalis stimulation depends on intrinsic acetylcholine

“…NB-induced CS-specific RF plasticity requires the engagement of muscarinic receptors in A1 (Miasnikov, McLin, & Weinberger, 2001). Similar cholinergically-based, muscarinic receptor-dependent CS-specific tuning shifts have been found in the bat, demonstrating species generality (Ji, Gao, & Suga, 2001;Ji & Suga, 2003;Ji, Suga, & Gao, 2005;Ma & Suga, 2005). NB-induced associative tuning shifts presumably consist of more cells becoming preferentially responsive to the CS frequency and thus to an increase in the area of CS representation might be expected, as it is in the case of learning-induced plasticity (Recanzone, Schreiner, & Merzenich, 1993;Rutkowski & Weinberger, 2005).…”

Cholinergic Modulation of Spindle Bursts in the Neonatal Rat Visual CortexIn Vivo

“…Acetylcholine (ACh) release correlated with EEG activation is responsible for behavioral arousal as first described by Magoun (1949, 1995) in their principle of "neocortical readiness state." The cholinergic system is involved in a large variety of cognitive processes (Damasio et al, 1985;Steriade et al, 1991;Everitt and Robbins, 1997) and gates sensory information processing (Singer, 1986;Juliano et al, 1991;Ma and Suga, 2005).…”

Bilateral Cortical Interaction: Modulation of Delay-Tuned Neurons in the Contralateral Auditory Cortex

“…The BF shifts (i.e., the change in the frequency map) in the AC evoked by focal electric stimulation of the AC are basically the same as those caused by auditory fear conditioning or a long repetitive tonal stimulation, although the cortical BF shift is long term for the conditioning but short term for the cortical electric stimulation Ma and Suga, 2003). This short-term cortical BF shift changes into a long-term BF shift when the cortical electric stimulation is accompanied with an application of acetylcholine to the AC (Ma and Suga, 2005) or with electric stimulation of the cholinergic basal forebrain . It has been hypothesized that the cortical short-term BF shift evoked by the cortical neural net and corticofugal feedback loop is augmented and changed into the long-term BF shift by activation of the cholinergic basal forebrain, which is activated by an acoustic stimulus becoming behaviorally relevant through conditioning (Gao and Suga, 1998;Suga and Ma, 2003).…”