Learning and memory involve the storage of specific sensory experiences. However, until recently the idea that the primary sensory cortices could store specific memory traces had received little ...attention. Converging evidence obtained using techniques from sensory physiology and the neurobiology of learning and memory supports the idea that the primary auditory cortex acquires and retains specific memory traces about the behavioural significance of selected sounds. The cholinergic system of the nucleus basalis, when properly engaged, is sufficient to induce both specific memory traces and specific behavioural memory. A contemporary view of the primary auditory cortex should incorporate its mnemonic and other cognitive functions.
Historically, sensory systems have been largely ignored as potential loci of information storage in the neurobiology of learning and memory. They continued to be relegated to the role of "sensory ...analyzers" despite consistent findings of associatively induced enhancement of responses in primary sensory cortices to behaviorally important signal stimuli, such as conditioned stimuli (CS), during classical conditioning. This disregard may have been promoted by the fact that the brain was interrogated using only one or two stimuli, e.g., a CSsuperscript + sometimes with a CSsuperscript -, providing little insight into the specificity of neural plasticity. This review describes a novel approach that synthesizes the basic experimental designs of the experimental psychology of learning with that of sensory neurophysiology. By probing the brain with a large stimulus set before and after learning, this unified method has revealed that associative processes produce highly specific changes in the receptive fields of cells in the primary auditory cortex (A1). This associative representational plasticity (ARP) selectively facilitates responses to tonal CSs at the expense of other frequencies, producing tuning shifts toward and to the CS and expanded representation of CS frequencies in the tonotopic map of A1. ARPs have the major characteristics of associative memory: They are highly specific, discriminative, rapidly acquired, exhibit consolidation over hours and days, and can be retained indefinitely. Evidence to date suggests that ARPs encode the level of acquired behavioral importance of stimuli. The nucleus basalis cholinergic system is sufficient both for the induction of ARPs and the induction of specific auditory memory. Investigation of ARPs has attracted workers with diverse backgrounds, often resulting in behavioral approaches that yield data that are difficult to interpret. The advantages of studying associative representational plasticity are emphasized, as is the need for greater behavioral sophistication.
The neural basis of auditory fear conditioning (AFC) is almost universally believed to be the amygdala, where auditory fear memories are reputedly acquired and stored. This widely-accepted amygdala ...model holds that the auditory conditioned stimulus (CS) and the nociceptive unconditioned stimulus (US) first converge in the lateral nucleus of the amygdala (AL), and are projected independently to it from the medial division of the medial geniculate nucleus (MGm) and the adjacent posterior intralaminar nucleus (PIN), which serve merely as sensory relays. However, the four criteria that are used to support the AL model, (a) CS–US convergence, (b) associative plasticity, (c) LTP and (d) lesion-induced learning impairment, are also met by the MGm/PIN. Synaptic and molecular approaches supporting the AL also implicate the MGm/PIN. As both the AL and its preceding MGm/PIN are critically involved, we propose that the latter be considered the “root” of AFC.
Historically, the primary auditory cortex has been largely ignored as a substrate of auditory memory, perhaps because studies of associative learning could not reveal the plasticity of receptive ...fields (RFs). The use of a unified experimental design, in which RFs are obtained before and after standard training (e.g., classical and instrumental conditioning) revealed associative representational plasticity, characterized by facilitation of responses to tonal conditioned stimuli (CSs) at the expense of other frequencies, producing CS-specific tuning shifts. Associative representational plasticity (ARP) possesses the major attributes of associative memory: it is highly specific, discriminative, rapidly acquired, consolidates over hours and days and can be retained indefinitely. The nucleus basalis cholinergic system is sufficient both for the induction of ARP and for the induction of specific auditory memory, including control of the amount of remembered acoustic details. Extant controversies regarding the form, function and neural substrates of ARP appear largely to reflect different assumptions, which are explicitly discussed. The view that the forms of plasticity are task dependent is supported by ongoing studies in which auditory learning involves CS-specific decreases in threshold or bandwidth without affecting frequency tuning. Future research needs to focus on the factors that determine ARP and their functions in hearing and in auditory memory.
Primary ("early") sensory cortices have been viewed as stimulus analyzers devoid of function in learning, memory, and cognition. However, studies combining sensory neurophysiology and learning ...protocols have revealed that associative learning systematically modifies the encoding of stimulus dimensions in the primary auditory cortex (A1) to accentuate behaviorally important sounds. This "representational plasticity" (RP) is manifest at different levels. The sensitivity and selectivity of signal tones increase near threshold, tuning above threshold shifts toward the frequency of acoustic signals, and their area of representation can increase within the tonotopic map of A1. The magnitude of area gain encodes the level of behavioral stimulus importance and serves as a substrate of memory strength. RP has the same characteristics as behavioral memory: it is associative, specific, develops rapidly, consolidates, and can last indefinitely. Pairing tone with stimulation of the cholinergic nucleus basalis induces RP and implants specific behavioral memory, while directly increasing the representational area of a tone in A1 produces matching behavioral memory. Thus, RP satisfies key criteria for serving as a substrate of auditory memory. The findings suggest a basis for posttraumatic stress disorder in abnormally augmented cortical representations and emphasize the need for a new model of the cerebral cortex.
Neuronal plasticity that develops in the cortex during learning is assumed to represent memory content, but the functions of such plasticity are actually unknown. The shift in spectral tuning in ...primary auditory cortex (A1) to the frequency of a tone signal is a compelling candidate for a substrate of memory because it has all of the cardinal attributes of associative memory: associativity, specificity, rapid induction, consolidation, and long-term retention. Tuning shifts increase the representational area of the signal in A1, as an increasing function of performance level, suggesting that area encodes the magnitude of acquired stimulus significance. The present study addresses the question of the specific function of learning-induced associative representational plasticity. We tested the hypothesis that specific increases in A1 representational area for an auditory signal serve the mnemonic function of enhancing memory strength for that signal. Rats were trained to bar-press for reward contingent on the presence of a signal tone (5.0 kHz), and assessed for memory strength during extinction. The amount of representational area gain for the signal frequency band was significantly positively correlated with resistance to extinction to the signal frequency in two studies that spanned the range of task difficulty. These findings indicate that specific gain in cortical representational area underlies the strength of the behaviorally-relevant contents of memory. Thus, mnemonic functions of cortical plasticity are determinable.
We hypothesized that learning-induced representational expansion in the primary auditory cortex (AI) directly encodes the degree of behavioral importance of a sound. Rats trained on an operant ...auditory conditioning task were variably motivated to the conditioned stimulus (CS) through different levels of water deprivation. Mean performance values correlated with deprivation level, validating them as a measure of the overall control and, therefore, behavioral importance of the CS. Electrophysiological mapping revealed expanded representations of the CS, compared with other frequencies in experimental subjects, but not in naive or visually trained controls that received noncontingent CS tones. Importantly, representational area showed a significant positive correlation with mean performance levels for only the CS band, with significant effects for relative area in contrast to only modest changes in absolute area. CS representational expansion was asymmetric into high-frequency zones, thus performance level also was significantly correlated with the relative anterior-posterior location of the enlarged representation. An increased representation of low frequencies, related to the acoustic spectrum of the reward delivery equipment, also was discovered in both experimental and control trained subjects, supporting the conclusion that behaviorally important sounds gain representational area. Furthermore, there was a surprising reduction in total AI area for the experimental and control groups, compared with untrained naive subjects, indicating that the functional dimensions of AI are not fixed. Overall, the findings support the encoding of acquired stimulus importance based on representational size in AI.
Learning alters the responses of neurons in the neocortex, typically strengthening their encoding of behaviorally relevant stimuli. These enhancements are studied extensively in the auditory cortex ...by characterizing changes in firing rates and evoked potentials. However, synchronous activity is also important for the processing of stimuli, especially the relationship between gamma oscillations in the local field potential and spiking. We investigated whether tone/shock fear conditioning in rats, a task known to alter responses in auditory cortex, also modified the relationship between gamma and unit activity. A boost in gamma oscillations developed, especially at sites tuned near the tone, and strengthened across multiple conditioning sessions. Unit activity became increasingly phase-locked to gamma, with sites tuned near the tone developing enhanced phase-locking during the tone, whereas those tuned away maintained a tendency to decrease their phase-locking. Enhancements in the coordination of spiking between sites tuned near the tone developed within the first conditioning session and remained throughout the rest of training. Enhanced cross-covariances in unit activity were strongest for subjects that exhibited robust conditioned fear. These results illustrate that changes in sensory cortex during associative learning extend to the coordination of neurons encoding the relevant stimulus, with implications for how it is processed downstream.
Gamma-band oscillations are a ubiquitous phenomenon in the nervous system and have been implicated in multiple aspects of cognition. In particular, the strength of gamma oscillations at the time a ...stimulus is encoded predicts its subsequent retrieval, suggesting that gamma may reflect enhanced mnemonic processing. Likewise, activity in the gamma-band can modulate plasticity in vitro. However, it is unclear whether experience-dependent plasticity in vivo is also related to gamma-band activation. The aim of the present study was to determine whether gamma activation in primary auditory cortex modulates both the associative memory for an auditory stimulus during classical conditioning and its accompanying specific receptive field plasticity. Rats received multiple daily sessions of single tone/shock trace and two-tone discrimination conditioning, during which local field potentials and multiunit discharges were recorded from chronically implanted electrodes. We found that the strength of tone-induced gamma predicted the acquisition of associative memory 24 h later and ceased to predict subsequent performance once asymptote was reached. Gamma activation also predicted receptive field plasticity that specifically enhanced representation of the signal tone. This concordance provides a long-sought link between gamma oscillations, cortical plasticity, and the formation of new memories.
Neurobiological theories of memory posit that the neocortex is a storage site of declarative memories, a hallmark of which is the association of two arbitrary neutral stimuli. Early sensory cortices, ...once assumed uninvolved in memory storage, recently have been implicated in associations between neutral stimuli and reward or punishment. We asked whether links between neutral stimuli also could be formed in early visual or auditory cortices. Rats were presented with a tone paired with a light using a sensory preconditioning paradigm that enabled later evaluation of successful association. Subjects that acquired this association developed enhanced sound evoked potentials in their primary and secondary visual cortices. Laminar recordings localized this potential to cortical Layers 5 and 6. A similar pattern of activation was elicited by microstimulation of primary auditory cortex in the same subjects, consistent with a cortico-cortical substrate of association. Thus, early sensory cortex has the capability to form neutral stimulus associations. This plasticity may constitute a declarative memory trace between sensory cortices.
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