Learning strategy determines auditory cortical plasticity

Learning modifies the primary auditory cortex (A1) to emphasize the processing and representation of behaviorally relevant sounds. However, the factors that determine cortical plasticity are poorly understood. While the type and amount of learning are assumed to be important, the actual strategies used to solve learning problems might be critical. To investigate this possibility, we trained two groups of adult male Sprague-Dawley rats to bar-press (BP) for water contingent on the presence of a 5.0 kHz tone using two different strategies: BP during tone presence or BP from tone-onset until receiving an error signal after tone cessation. Both groups achieved the same high levels of correct performance and both groups revealed equivalent learning of absolute frequency during training. Post-training terminal "mapping" of A1 showed no change in representational area of the tone signal frequency but revealed other substantial cue-specific plasticity that developed only in the tone-onset-to-error strategy group. Threshold was decreased approximately 10 dB and tuning bandwidth was narrowed by approximately 0.7 octaves. As sound onsets have greater perceptual weighting and cortical discharge efficacy than continual sound presence, the induction of specific learning-induced cortical plasticity may depend on the use of learning strategies that best exploit cortical proclivities. The present results also suggest a general principle for the induction and storage of plasticity in learning, viz., that the representation of specific acquired information may be selected by neurons according to a match between behaviorally selected stimulus features and circuit/network response properties.     

Long-term consolidation and retention of learning-induced tuning plasticity in the auditory cortex of the guinea pig.

The major goal of this study was to determine whether classical conditioning produces long-term neural consolidation of frequency tuning plasticity in the auditory cortex. Local field potentials (LFPs) were obtained from chronically implanted adult male Hartley guinea pigs that were divided into conditioning (n = 4) and sensitization control (n = 3) groups. Tuning functions were determined in awake subjects for average LFPs (approximately 0.4 to 36.0 kHz, -20 to 80 dB) immediately before training as well as 1 h and 1, 3, 7, and 10 days after training; sensitization subjects did not have a 10-day retention test. Conditioning consisted of a single session of 30 to 45 trials of a 6-s tone (CS, 70 dB) that was not the best frequency (BF, peak of a tuning curve), followed by a brief leg shock (US) at CS offset. Sensitization control animals received the same density of CS and US presentations unpaired. Heart rate recordings showed that the conditioning group developed conditioned bradycardia, whereas the sensitization control group did not. Local field potentials in the conditioning group, but not in the sensitization group, developed tuning plasticity. The ratio of responses to the CS frequency versus the BF were increased 1 h after training, and this increase was retained for the 10-day period of the study. Both tuning plasticity and retention were observed across stimulus levels (10-80 dB). Most noteworthy, tuning plasticity exhibited consolidation (i.e., developed greater CS-specific effects across retention periods), attaining asymptote at 3 days. The findings indicate that LFPs in the auditory cortex have three cardinal features of behavioral memory: associative tuning plasticity, long-term retention, and long-term consolidation. Potential cellular and subcellular mechanisms of LFP tuning plasticity and long-term consolidation are discussed.     

The nucleus basalis and memory codes: auditory cortical plasticity and the induction of specific, associative behavioral memory

Receptive field (RF) plasticity develops in the primary auditory cortex (ACx) when a tone conditioned stimulus (CS) becomes associated with an appetitive or aversive unconditioned stimulus (US). This prototypical stimulus-stimulus (S-S) association is accompanied by shifts of frequency tuning of neurons toward or to the frequency of the CS such that the area of best tuning of the CS frequency is increased in the tonotopic representation of the ACx. RF plasticity has all of the major characteristics of behavioral associative memory: it is highly specific, discriminative, rapidly induced, consolidates (becomes stronger and more specific over hours to days) and can be retained indefinitely (tested to two months). Substitution of nucleus basalis (NB) stimulation for a US induces the same associative RF plasticity, and this requires the engagement of muscarinic receptors in the ACx. Pairing a tone with NB stimulation actually induces specific, associative behavioral memory, as indexed by post-training frequency generalization gradients. The degree of acquired behavioral significance of sounds appears to be encoded by the number of neurons that become retuned in the ACx to that acoustic stimulus, the greater the importance, the greater the number of re-tuned cells. This memory code has recently been supported by direct neurobehavioral tests. In toto, these findings support the view that specific, learned auditory memory content is stored in the ACx, and further that this storage of information during learning and the instantiation of the memory code involves the engagement of the nucleus basalis and its release of acetylcholine into target structures, particularly the cerebral cortex.     

Signal clustering modulates auditory cortical activity in humans

Auditory streaming and its relevance to attentional processing was examined using event-related brain potentials (ERPs) in situations facilitating perception of one or two streams of sounds. Subjects listened to sequences of brief tones of three different frequencies presented in random order. In evenly spaced (ES) conditions, the three frequencies were equidistant on the musical scale. In clustered, easy (CE) conditions, the attended frequency was distinct, while the middle and extreme distractor tones were clustered together. In clustered, hard (CH) conditions, the attended frequency was clustered with one of the distractors. The subjects pressed a button in response to occasional target tones of longer duration at a prespecified frequency. The subjects were faster and more accurate in CE conditions than they were in ES conditions, and ERP attention effects were enhanced in amplitude in CE conditions. Conversely, the subjects were slower and less accurate in CH conditions and ERP attention effects were delayed in latency and decreased in amplitude. Clustering effects suggest that the processing of stimuli belonging to the attended stream was promoted and the processing of those falling outside the stream was inhibited. The timing and scalp distribution of clustering-related changes in ERPs suggest that clustering modulates early sensory processing in auditory cortex.     

Lifespan differences in cortical dynamics of auditory perception

Using electroencephalographic recordings (EEG), we assessed differences in oscillatory cortical activity during auditory‐oddball performance between children aged 9–13 years, younger adults, and older adults. From childhood to old age, phase synchronization increased within and between electrodes, whereas whole power and evoked power decreased. We conclude that the cortical dynamics of perceptual processing undergo substantial reorganization from childhood to old age, and discuss possible reasons for the inverse relation between age trends in phase synchronization and power, such as lifespan differences in neural background activity, or a lifespan shift from rate coding in children to temporal coding in adults.     

Reduction in auditory distraction by retrieval strategy

Most research on auditory distraction on task performance focuses on those features of the sound that determine a drop in efficiency, with scant regard for examining the processing properties inherent in the focal task. We report how one such property, retrieval strategy, can also influence the degree of disruption by background sound. Using a task that called for the retrieval of realistic train journey information, we showed that retrieval by categories of verbal sequences was not susceptible to disruption by office sound - 65-75 dB(A). However, versions of the task requiring either free or serial recall showed evidence of disruption, a pattern of results consistent with the changing-state account of the irrelevant sound effect, which highlights the key role of serial rehearsal in determining disruption.     

Spatial summation in the evoked cortical response to auditory stimuli

Six Ss were presented monaurally and binaurally with stimuli of 0.5, 2.0, and 4.0 kHz at 40 and 70 dB sensation levels. Their computer averaged evoked potentials indicated substantially larger amplitudes (N₁ -P₂) with bilateral stimulation, regardless of frequency. Stimulation at 70 dB SL gave greater responses than that to 40 dB.     

Environmental enrichment improves behavioral performance and auditory spatial representation of primary auditory cortical neurons in rat

Environmental enrichment (EE) has an important role in brain plasticity. Early research has shown that EE increases the response strength of neurons in the auditory cortex, but it remains unknown whether EE can influence the process of spatial localization in the auditory system. In this study, we raised rats in enriched and standard conditions from postnatal day 10 to day 56. By testing behavioral tasks via auditory cues, we have shown that EE improved the number of correct scores, but decreased the reaction time and azimuth deviation in behavioral performance of sound-azimuth discrimination. By in vivo extracellular recording, we have shown that EE enhanced the directional sensitivity of neurons in the primary auditory cortex. For example, EE rats had a smaller spatial receptive field, sharper frequency tuning curve and directional selective curve of auditory neurons compared with normal rats. Our findings indicate that early exposure to EE increases directional sensitivity. These results provide an insight into developmental plasticity in the auditory system.     

Associative representational plasticity in the auditory cortex: a synthesis of two disciplines

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 CS(+) sometimes with a CS(-), 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.     

Learning in a task of complex auditory streaming and identification

Adult humans were studied for improvements in their ability to segregate natural whole speech in background noise, in 6 test sessions spaced with a very wide range of inter-session interval (ISI) ranging from minutes to weeks apart so as to examine the effect of this parameter on initial (early) and late components of perceptual learning. Improvements were found even with spacings of 3 weeks between the punctate task sessions. All subjects showed similar total learning amounts but there were sex- and ISI-dependent differences in learning patterns, which we indexed by dividing the overall exponentially-decreasing learning pattern into an early phase between the first two sessions and a later phase between the second and sixth sessions. Males tested at all ISIs and females tested at short (2, 5 and 15 min) and long (1–21 days) ISIs showed small amounts of early-phase learning and large amounts of late-phase learning. However, females tested at intermediate (30 min and 1 h) ISIs showed only early learning, i.e., faster learning given that the total learning was the same. This sex- and ISI-specific deviant pattern could be changed to the standard pattern by interposing an overnight interruption that included sleep amongst test sessions. Thus, improvement in this complex auditory streaming and identification task can occur even with very brief and widely-spaced exposure, generally through a standard pattern of slower overall learning, but also through a sex- and ISI-specific deviant pattern of very rapid early learning which can be modulated by interposed delay unlike the standard pattern.     

Learning to map: strategy discovery and strategy change in young children

A series of microgenetic experiments was conducted to examine the role of experience on 2.5- to 5-year-old children's discovery of spatial mapping strategies. With experience, 3- to 4-year-olds discovered a strategy for mapping corresponding locations that shared both featural and spatial similarities. When featural and spatial correspondences were placed in conflict, requiring children to negotiate both object-centered and location-centered mapping possibilities, 4- to 5-year-olds proved capable of discovering a novel mapping strategy, abandoning an ineffective strategy, and generalizing the acquired strategy across analogous tasks. Upon examining the mechanisms underlying developmental differences in strategy discovery and strategy change, the author observed that 3 key components contributed to the children's spatial mapping skills: encoding locations within each space, noticing a potential analogy between spaces, and detecting precise mapping correspondences.     

Chemical plasticity of visual cortical neurons in integrative organization of feeding behavior in cats

The P.K. Anokhin conception of organization of systemic behavior was used to study the discharge activity and chemical plasticity of cortical neurons in a goal-directed behavior. Chemical sensitivity of neurons in the visual cortex of instrumentally conditioned cats was studied during successive stages of food procuring and consuming. The results showed that definite stages of this integrated behavioral act are characterized by differences in the chemical sensitivity of visual neurons to neurotransmitters. The largest number of neurons resistant to neurotransmitters was found among cells that did not respond at successive stages of goal-directed behavior. The iontophoretic delivery of cycloheximide and lyzilvasopressine altered the discharge activity of individual cortical neurons at different stages of stereotyped instrumental conditioned acts. This suggests that the integrative organization of the feeding behavior is determined by chemical plasticity of the brain’s visual cortical neurons and is dependent upon the processes of protein synthesis. According to the functional system theory (Anokhin, 1974) each brain neuron is included, by various degrees of freedom, in the stages of systemic organization that underlie the goal-directed behavior. Thanks to the plastic reorganization of brain units, each stage is directed toward the achievement of useful adaptive results for the organism during interaction with different environmental factors (Adrianov, 1993; Fadeev, 1988). It may be proposed that the reorganization of discharges of brain neurons that occurs at different stages of activity is due to changes in their chemical capacities. In concordance with such a hypothesis, the purpose of the present investigation was to study the chemical sensitivity of single visual cortical neurons to neurotransmitters at different stages of systemic organization of feeding behavior. The influence of protein synthesis inhibitors on the sensitivity of cortical neurons was also investigated.     

Learning strategy differentially impacts memory connections in children and adults

Even once children can accurately remember their experiences, they nevertheless struggle to use those memories in flexible new ways—as in when drawing inferences. However, it remains an open question as to whether the developmental differences observed during both memory formation and inference itself represent a fundamental limitation on children's learning mechanisms, or rather their deployment of suboptimal strategy. Here, 7–9-year-old children (N = 154) and young adults (N = 130) first formed strong memories for initial (AB) associations and then engaged in one of three learning strategies as they viewed overlapping (BC) pairs. We found that being told to integrate—combine ABC during learning—both significantly improved children's ability to explicitly relate the indirectly associated A and C items during inference and protected the underlying pair memories from forgetting. However, this finding contrasted with implicit evidence for memory-to-memory connections: Adults and children both formed A-C links prior to any knowledge of an inference test—yet for children, such links were most apparent when they were told to simply encode BC, not integrate. Moreover, the accessibility of such implicit links differed between children and adults, with adults using them to make explicit inferences but children only doing so for well-established direct AB pairs. These results suggest that while a lack of integration strategy may explain a large share of the developmental differences in explicit inference, children and adults nevertheless differ in both the circumstances under which they connect interrelated memories and their ability to later leverage those links to inform flexible behaviours.

Research Highlights

• Children and adults view AB and BC pairs related through a shared item, B. This provides an opportunity for learners to connect A–C in memory.
• Being encouraged to integrate ABC during learning boosted performance on an explicit test of A–C connections (children and adults) and protected from forgetting (children).
• Children and adults differed in when implicit A–C connections were formed—occurring primarily when told to separately encode BC (children) versus integrate (adults), respectively.
• Adults used implicit A–C connections to facilitate explicit judgments, while children did not. Our results suggest developmental differences in the learning conditions promoting memory-to-memory connections.

     

Lack of strategy holding: A new pattern of learning deficit in cortical dementias

The aim of this study was to demonstrate, by means of systematic research and qualitative data analysis, the presence, among a group of patients with fronto‐temporal lobar degeneration of a subgroup that, at variance with the standard pattern, is able to devise and implement learning strategies, but appear impaired at carrying them on from a trial to the next. In order to provide evidence of the existence of a group of patients showing this type of learning disability, that we refer to as lack of strategy holding, we performed a stepwise hierarchical cluster analysis of a set of variables whose scores were selected from the subject's performance at the Test de Aprendizaje Verbal España‐Complutense. Results substantiate the segregation of three groups of subjects characterized by the following patterns of performance: normal elderly individuals, who show a quite preserved ability to discover a semantic strategy along the learning trials and to carry it from a trial to the next, patients presenting with a deficit in implementing semantic learning strategies and possibly use of serial and/or phonological strategies to perform the task, and to patients who, although able to generate and implement appropriate learning strategies, appear unable to carry them over the learning trials. The presence of this new pattern raises a few questions that seem worth trying to address.