Frequency-specific receptive field plasticity in the medial geniculate body induced by Pavlovian fear conditioning is expressed in the anesthetized brain.

Fear conditioning modifies the processing of frequency information; receptive fields (RFs) in the auditory cortex and the medial geniculate body (MGB) are altered to favor processing the frequency of the conditioned stimulus/stimuli (CS) over the pretraining best frequency (BF) and other frequencies. This experiment was designed to determine whether brief conditioning in the waking state produces RF plasticity that is expressed under general anesthesia. Guinea pigs bearing electrodes in the MGB received 20 trials on tone-shock pairing in a single training session. RFs were determined with animals under ketamine anesthesia before conditioning and 1–3 hrs and 24 hrs after conditioning. Frequency-specific RF plasticity was evident for both postconditioning periods: The BF shifted toward or to the CS frequency, responses to the BF decreased, and responses to the CS increased. Broadly tuned cells developed greater RF plasticity than narrowly tuned neurons. Results demonstrate that the specific neuronal results of brief learning experiences can be expressed in the anesthetized brain. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Response characteristics of neurons in the medial component of the medial geniculate nucleus during Pavlovian differential fear conditioning in rabbits.

The amygdaloid central nucleus (ACE) may contribute significantly to Pavlovian fear-conditioned bradycardic responses during the presentation of conditioned emotional stimuli. Because the medial component of the medial geniculate nucleus (MGm) is a major source of input to the region of the ACE, the extracellular single-unit responses of MGm neurons were examined during Pavlovian differentially conditioned bradycardic responding in rabbits. Conditioning involved pairing one tone (CS+) with paraorbital shock and presenting another tone (CS–) in the absence of shock. Two general classes of MGm neurons were identified based on their conditioned-response characteristics. One group responded with greater increases in activity and at a shorter latency to the CS+ compared with the CS–, whereas the other group responded with greater increases in activity and at a shorter latency to the CS– compared with the CS+. Recordings from MGm neurons in naive rabbits prior to conditioning provided evidence that the acoustic stimuli used subsequently as the CS+ and CS– did not evoke differential responses. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Stimulation at a site of auditory-somatosensory convergence in the medial geniculate nucleus is an effective unconditioned stimulus for fear conditioning.

The medial division of the medial geniculate nucleus (MGm) and the posterior intralaminar nucleus (PIN) are necessary for conditioning to an auditory conditioned stimulus/stimuli (CS), receive both auditory and somatosensory input, and project to the amygdala, which is involved in production of fear conditioned responses (CRs). If CS–unconditioned stimulus (UCS) convergence in the MGm-PIN is critical for fear conditioning, then microstimulation of this area should serve as an effective UCS during classical conditioning, in place of standard footshock. Guinea pigs underwent conditioning (40–60 trials) using a tone as the CS and medial geniculate complex microstimulation as the UCS. Conditioning bradycardia developed when the UCS electrodes were in the PIN. However, microstimulation was not an effective UCS for conditioning in other parts of the medial geniculate or for sensitization training in the PIN or elsewhere. Learning curves were similar to those found previously for footshock UCS. Thus, the PIN can be a locus of functional CS–UCS convergence for fear conditioning to acoustic stimuli. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Induction of receptive field plasticity in the auditory cortex of the guinea pig during instrumental avoidance conditioning.

Classical tone conditioning shifts frequency tuning in the auditory cortex to favor processing of the conditioned stimulus (CS) frequency versus other frequencies. This receptive field (RF) plasticity is associative, highly specific, rapidly acquired, and indefinitely retained—all important characteristics of memory. The investigators determined whether RF plasticity also develops during instrumental learning. RFs were obtained before and up to 24 hr after 1 session of successful 1-tone avoidance conditioning in guinea pigs. Long-term RF plasticity developed in all subjects (N?=?6). Two-tone discrimination training also produced RF plasticity, like classical conditioning. Because avoidance responses prevent full elicitation of fear by the CS, long-term RF plasticity does not require the continual evocation of fear, suggesting that neural substrates of fear expression are not essential to RF plasticity. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Appetitive conditioning-induced plasticity is expressed during paradoxical sleep in the medial geniculate, but not in the lateral amygdala.

This study examined whether neurons in the medial division of the medial geniculate (MGm) and the dorsal part of the lateral amygdala (LAd) express learning-induced plasticity in paradoxical sleep (PS) after appetitive conditioning, as they do in PS after fear conditioning. Rats received tone-food pairings in 3 sessions. After each session, the tone was presented at a nonawakening intensity during PS. Multiunit activity was simultaneously recorded in MGm and LAd. During waking, increases in tone-evoked discharges developed in MGm and LAd; however, as training continued, they lessened in LAd, but not in MGm. During PS, conditioned tone responses were expressed in MGm, but not in LAd. Thus, these results demonstrate dissociation of MGm and LAd plasticity. Moreover, compared with fear conditioning results, they suggest that expression of amygdalar plasticity in PS depends on the emotional salience of the stimulus. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Heterosynaptic long-term facilitation of sensory-evoked responses in the auditory cortex by stimulation of the magnocellular medial geniculate body in guinea pigs.

The magnocellular nucleus of the medial geniculate body (MGm) develops physiological plasticity during classical conditioning and may be involved in learning-induced receptive field plasticity in the auditory cortex. To determine the ability of the MGm to produce long-term modification of evoked activity in the auditory cortex, the experimenters paired electrical stimulation of the MGm with preceding clicks in adult guinea pigs under barbiturate anesthesia. The amplitudes of average click-evoked potentials were significantly facilitated in all Ss. Facilitation endured for 2 hrs, the maximum duration of recording. Sham-stimulated control guinea pigs did not develop facilitation. Thus, a nonlemniscal thalamic sensory nucleus can produce enduring facilitation of sensory-evoked activity in primary sensory cortex, suggesting that long-term physiological plasticity in the sensory cortex during learning may involve nonlemniscal thalamic mechanisms. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Fear conditioning-induced plasticity in auditory thalamus and cortex: To what extent is it expressed during slow-wave sleep?

After fear conditioning to a tone, rats received nonawakening presentations of the tone alone during slow-wave sleep (SWS) episodes. Multiunit activity was recorded in the medial part of the medial geniculate (MGm) and in the primary auditory cortex (ACx). Although tone-evoked responses were increased in MGm and ACx during the 3 conditioning sessions, group data failed to show any significant changes during SWS. Nonetheless, the few recordings (5/29) that exhibited the strongest conditioned responses during wakefulness expressed enhanced responding during SWS. Compared with previous data obtained in MGm during paradoxical sleep, associative plastic changes were less easily expressed during SWS. These results are discussed with regard to functional changes that occur in the thalamocortical system across vigilance states. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Receptive field plasticity in the auditory cortex during frequency discrimination training: Selective retuning independent of task difficulty.

Classical conditioning is known to induce frequency-specific receptive field (RF) plasticity in the auditory cortex (ACx). This study determined the effects of discrimination training on RFs at 2 levels of task difficulty. Single unit and cluster discharges were recorded in the ACx of adult guinea pigs trained in a tone-shock frequency discrimination paradigm (30 intermixed trials each of positive CS [CS+]-shock and negative CS [CS–] alone) with behavioral performance indexed by the cardiac deceleration CR. After training in an easy task in which Ss developed discriminative CRs, they were trained in a difficult task (reduced frequency distance between CS+ and CS–) in which they failed to discriminate. However, frequency-specific RF plasticity developed at both levels of task difficulty. Responses to the frequency of the CS+ were increased, whereas responses to other frequencies, including the CS– and the prepotent best frequency (BF) were reduced. In many cases, tuning was shifted such that the frequency of the CS+ became the new BF. The effects were present or stronger after a 1-hr retention interval. The role of RF plasticity in the ACx is discussed for behavioral performance and information storage. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Role of context in the expression of learning-induced plasticity of single neurons in auditory cortex.

Classical conditioning produces frequency-specific plasticity of receptive fields (RFs) of single neurons in cat auditory cortex (D. M. Diamond and N. M. Weinberger; see record 1987-14817-001). In this article we show that although plasticity may be observed during both training trials and determination of RFs, it is usually expressed in a qualitatively different form (e.g., decreased response during conditioning vs. increased response to this same conditioned stimulus in the postconditioning RF). This differential expression of learning-induced plasticity provides evidence for a role of context in neurophysiological mechanisms of learning in auditory cortex. A model of cortical neurons functioning within a mosaic of influences is presented. The Functional Mosaic model views the induction and expression of plasticity as separate processes. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Single neurons in the medial prefrontal cortex of the rat exhibit tonic and phasic coding during trace fear conditioning.

Trace fear conditioning is a learning task that requires the association of an auditory conditioned stimulus (CS) and a shock unconditioned stimulus (US) that are separated by a 20-s trace interval. Single neuron activity was recorded from the prelimbic and infralimbic areas of the medial prefrontal cortex in rats during trace fear conditioning or nonassociative unpaired training. Prelimbic neurons showed learning-related increases in activity to the CS and US, whereas infralimbic neurons showed learning-related decreases in activity to these stimuli. A subset of prelimbic neurons exhibited sustained increases in activity during the trace interval. These sustained prelimbic responses may provide a bridging code that allows for overlapping representations of CS and US information within the trace fear conditioning circuit. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Learning-induced physiological memory in adult primary auditory cortex: receptive fields plasticity, model, and mechanisms

It is well established that the functional organization of adult sensory cortices, including the auditory cortex, can be modified by deafferentation, sensory deprivation, or selective sensory stimulation. This paper reviews evidence establishing that the adult primary auditory cortex develops physiological plasticity during learning. Determination of frequency receptive fields before and at various times following aversive classical conditioning and instrumental avoidance learning in the guinea pig reveals increased neuronal responses to the pure tone frequency used as a conditioned stimulus (CS). In contrast, responses to the pretraining best frequency and other non-CS frequencies are decreased. These opposite changes are often sufficient to shift cellular tuning toward or even to the frequency of the CS. Learning-induced receptive field (RF) plasticity (i) is associative (requires pairing tone and shock), (ii) highly specific to the CS frequency (e.g., limited to this frequency +/- a small fraction of an octave), (iii) discriminative (specific increased response to a reinforced CS+ frequency but decreased response to a nonreinforced CS- frequency), (iv) develops extremely rapidly (within 5 trials, the fewest trials tested), and (v) is retained indefinitely (tested to 8 weeks). Moreover, RF plasticity is robust and not due to arousal, but can be expressed in the deeply anesthetized subject. Because learning- induced RF plasticity has the major characteristics of associative memory, it is therefore referred to as "physiological memory". We developed a model of RF plasticity based on convergence in the auditory cortex of nucleus basalis cholinergic effects acting at muscarinic receptors, with lemniscal and nonlemniscal frequency information from the ventral and magnocellular divisions of the medial geniculate nucleus, respectively. In the model, the specificity of RF plasticity is dependent on Hebbian rules of covariance. This aspect was confirmed in vivo using microstimulation techniques. Further, the model predicts that pairing a tone with activation of the nucleus basalis is sufficient to induce RF plasticity similar to that obtained in behavioral learning. This prediction has been confirmed. Additional tests of the model are described. RF plasticity is thought to translate the acquired significance of sound into an increased frequency representation of behaviorally important stimuli.     

Physiological memory in primary auditory cortex: characteristics and mechanisms

"Physiological memory" is enduring neuronal change sufficiently specific to represent learned information. It transcends both sensory traces that are detailed but transient and long-term physiological plasticities that are insufficiently specific to actually represent cardinal details of an experience. The specificity of most physiological plasticities has not been comprehensively studied. We adopted receptive field analysis from sensory physiology to seek physiological memory in the primary auditory cortex of adult guinea pigs. Receptive fields for acoustic frequency were determined before and at various retention intervals after a learning experience, typified by single-tone delay classical conditioning, e.g., 30 trials of tone-shock pairing. Subjects rapidly (5-10 trials) acquire behavioral fear conditioned responses, indexing acquisition of an association between the conditioned and the unconditioned stimuli. Such stimulus-stimulus association produces receptive field plasticity in which responses to the conditioned stimulus frequency are increased in contrast to responses to other frequencies which are decreased, resulting in a shift of tuning toward or to the frequency of the conditioned stimulus. This receptive field plasticity is associative, highly specific, acquired within a few trials, and retained indefinitely (tested to 8 weeks). It thus meets criteria for "physiological memory." The acquired importance of the conditioned stimulus is thought to be represented by the increase in tuning to this stimulus during learning, both within cells and across the primary auditory cortex. Further, receptive field plasticity develops in several tasks, one-tone and two-tone discriminative classical and instrumental conditioning (habituation produces a frequency-specific decrease in the receptive field), suggesting it as a general process for representing the acquired meaning of a signal stimulus. We have proposed a two-stage model involving convergence of the conditioned and unconditioned stimuli in the magnocellular medial geniculate of the thalamus followed by activation of the nucleus basalis, which in turn releases acetylcholine that engages muscarinic receptors in the auditory cortex. This model is supported by several recent findings. For example, tone paired with NB stimulation induces associative, specific receptive field plasticity of at least a 24-h duration. We propose that physiological memory in auditory cortex is not "procedural" memory, i.e., is not tied to any behavioral conditioned response, but can be used flexibly.     

Rapid development of learning-induced receptive field plasticity in the auditory cortex.

Classical conditioning induces frequency-specific receptive field (RF) plasticity in the auditory cortex after relatively brief training (30 trials), characterized by increased response to the frequency of the CS and decreased responses to other frequencies, including the pretraining best frequency (BF). This experiment determined the development of this CS-specific RF plasticity. Guinea pigs underwent classical conditioning to a tonal frequency, and receptive fields of neurons in the auditory cortex were determined before and after 5, 15, and 30 CS–UCS (unconditioned stimulus) pairings, as well as 1 hr posttraining. Highly selective RF changes were observed as early as the first 5 training trials. They culminated after 15 trials, then stabilized after 30 trials and 1 hr posttraining. The rapid development of RF plasticity satisfies a criterion for its involvement in the neural bases of a specific associative memory. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Neuronal plasticity induced by fear conditioning is expressed during paradoxical sleep: Evidence from simultaneous recordings in the lateral amygdala and the medial geniculate in rats.

The lateral amygdala (LA) and its afferent connections from the medial geniculate (MG) play a pivotal role in auditory fear conditioning. The authors evaluated whether those neurons could express in paradoxical sleep (PS) physiological plasticity acquired in waking. After a habituation session, rats received tone–footshock pairings in 3 sessions. After each session, the tone alone was presented during PS episodes. Multiunit activity was simultaneously recorded in the LA and the medial part of the MG. Both in LA and MG, conditioned responses emerged rapidly (within 5 trials), were expressed with short latency (     

Normal conditioning inhibition and extinction of freezing and fear-potentiated startle following electrolytic lesions of medial prefrontal cortex in rats.

The authors investigated the role of medial prefrontal cortex (mPFC) in the inhibition of conditioned fear in rats using both Pavlovian extinction and conditioned inhibition paradigms. In Experiment 1, lesions of ventral mPFC did not interfere with conditioned inhibition of the fear-potentiated startle response. In Experiment 2, lesions made after acquisition of fear conditioning did not retard extinction of fear to a visual conditioned stimulus (CS) and did not impair "reinstatement" of fear after unsignaled presentations of the unconditioned stimulus. In Experiment 3, lesions made before fear conditioning did not retard extinction of fear-potentiated startle or freezing to an auditory CS. In both Experiments 2 and 3, extinction of fear to contextual cues was also unaffected by the lesions. These results indicate that ventral mPFC is not essential for the inhibition of fear under a variety of circumstances. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Basal forebrain stimulation induces discriminative receptive field plasticity in the auditory cortex.

Learning alters receptive field (RF) tuning in the primary auditory cortex (ACx) to emphasize the frequency of a tonal conditioned stimulus. RF plasticity is a candidate substrate of memory, as it is associative, specific, discriminative, rapidly induced, and enduring. The authors hypothesized that it is produced by the release of acetylcholine in the ACx from the basal forebrain (BasF), caused by presentation of reinforced but not nonreinforced conditioned stimuli. Waking adult male Hartley guinea pigs (n?=?16) received 1 of 2 tones followed by BasF stimulation, in a single session of 30 pseudo-random order trials each. RFs from neuronal discharges before and after differential pairing revealed the induction of predicted plasticity, as well as increased responses to the paired tone and decreased responses to the unpaired tone. Thus, highly specific, learning-induced RF plasticity in the ACx may be produced by activation of the BasF by a reinforced conditioned stimulus. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Physiological plasticity of single neurons in auditory cortex of the cat during acquisition of the pupillary conditioned response: II. Secondary field (AII).

Recorded the discharges of 22 single neurons in the secondary auditory cortical field (AII) during acquisition of the pupillary dilation conditioned defensive response in 12 chronically prepared cats. All 22 neurons developed discharge plasticity in background activity, and 21 of 22 cells developed plasticity in their responses to the acoustic CS. Decreases in background activity developed at the time that Ss began to display CRs. Increases in background activity developed in Ss that became more tonically aroused during conditioning. However, both increases and decreases in evoked activity developed independently of the rate of pupillary learning, tonic arousal level, or changes in background activity. Findings indicate that changes in background activity are closely related to behavioral processes of learning and arousal, whereas stimulus-evoked discharge plasticity develops solely as a consequence of stimulus pairing. Comparison with data obtained by the 2nd author and colleagues (see record 1985-03305-001) for the primary auditory cortical field (AI) indicates that both regions developed neuronal discharge plasticity early in the conditioning phase and that increases in background activity in primary auditory cortex were also associated with elevated levels of tonic arousal. The incidence of single neurons developing learning-related discharge plasticity was significantly greater in AII than in AI. Findings are discussed in terms of parallel processing in sensory systems and multiple sensory cortical fields. (69 ref) (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Neuronal activity in the medial prefrontal cortex during Pavlovian eyeblink and nictitating membrane conditioning

The present study assessed Pavlovian eyeblink (EB) conditioning, using tones and periorbital shock as the conditioned and unconditioned stimuli (CS and US), and nictitating membrane (NM) conditioning, using tones and airpuffs as the CS and US. During each experiment, CS-evoked changes in multiple-unit activity (MUA) in the medial prefrontal cortex (mPFC) were recorded. Concomitant heart rate (HR) conditioned responses (CRs) were also recorded. A nonassociative control group received explicitly unpaired presentations of the CS and US in each experiment. Increases in both NM and EB CRs occurred over sessions in the paired, but not the unpaired, groups. Decelerative HR CRs also occurred in the eyeshock, but not the airpuff, group. Although tone-evoked increases in neuronal activity were obtained during 10 initial tone-alone presentations in all groups, this activity habituated over trials. CS-evoked increases in neuronal activity also occurred, but this activity was considerably greater in the group that received periorbital shock as the US. During subsequent extinction trials, decreases in tone-evoked neuronal activity occurred in this group, compared with the previous CS/US paired trials. CS-evoked MUA increases were minimal during all except the pretraining phase of the study in the CS/US unpaired control groups and in the paired airpuff group. These findings show that neuronal activity during associative learning occurs in the mPFC during Pavlovian EB, as well as HR conditioning, but this activity apparently reflects an affective component to learning that is only indirectly related to skeletal conditioning.     

Disruptive effects of posttraining perirhinal cortex lesions on conditioned fear: Contributions of contextual cues.

Lesions placed in the rostral perirhinal cortex (rPRh) after fear conditioning interfere with the expression of conditioned fear responses elicited by auditory and visual conditioned stimuli when these stimuli are presented in a context that differs from the conditioning context. The present study examined whether lesions of the rPRh have similar effects when animals are tested in the conditioning context. Two days after male rats received classical fear conditioning, involving the pairing of an auditory CS with footshock, bilateral electrolytic lesions were produced in the rPRh. Five days later conditioned freezing behavior was measured during a 60-s exposure to the CS in a novel context and then 1 hr later in the conditioning context. There were 3 major findings: rPRh-lesioned Ss froze significantly less than controls to the CS in the novel context, thus confirming previously reported findings. rPRh-lesioned Ss also froze less than controls to the CS in the conditioning context, but froze significantly more to the CS in the conditioning than in the novel context, suggesting that at least part of the deficit in the novel context is due to the absence of contextual cues. Ss with rPRh lesions froze significantly less than controls to the conditioning context itself.… (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Learning-induced plasticity in the medial geniculate nucleus is expressed during paradoxical sleep.

Fear conditioning to an acoustic stimulus produces increases in tone-evoked discharges of neurons in the medial division of the medial geniculate nucleus (MG). This study examined the responses of MG neurons to a conditioned tone presented in paradoxical sleep (PS). After 1 session of habituation to a tone, awake rats underwent conditioning in 3 sessions during which the tone was used as the CS preceding a footshock. Control rats received unpaired presentations of tone and shock. The same tone, which never awakened the animal, was presented during PS following each daily session. Responses of MG neurons to the tone in PS were increased after conditioning. This enhancement was as large as that in waking and was manifested earlier after tone onset than in waking. No change appeared after pseudoconditioning. These results demonstrate that associatively induced plasticity in the MG can be expressed during PS. (PsycINFO Database Record (c) 2010 APA, all rights reserved)