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Cerebral Cortex (New York, N.Y. : 1991) Dec 2019Rapid and flexible learning during behavioral choices is critical to our daily endeavors and constitutes a hallmark of dynamic reasoning. An important paradigm to...
Rapid and flexible learning during behavioral choices is critical to our daily endeavors and constitutes a hallmark of dynamic reasoning. An important paradigm to examine flexible behavior involves learning new arbitrary associations mapping visual inputs to motor outputs. We conjectured that visuomotor rules are instantiated by translating visual signals into actions through dynamic interactions between visual, frontal and motor cortex. We evaluated the neural representation of such visuomotor rules by performing intracranial field potential recordings in epilepsy subjects during a rule-learning delayed match-to-behavior task. Learning new visuomotor mappings led to the emergence of specific responses associating visual signals with motor outputs in 3 anatomical clusters in frontal, anteroventral temporal and posterior parietal cortex. After learning, mapping selective signals during the delay period showed interactions with visual and motor signals. These observations provide initial steps towards elucidating the dynamic circuits underlying flexible behavior and how communication between subregions of frontal, temporal, and parietal cortex leads to rapid learning of task-relevant choices.
Topics: Adolescent; Adult; Association Learning; Brain; Child; Female; Frontal Lobe; Humans; Male; Middle Aged; Motor Activity; Neural Pathways; Neurons; Parietal Lobe; Photic Stimulation; Psychomotor Performance; Temporal Lobe; Visual Perception; Young Adult
PubMed: 30590542
DOI: 10.1093/cercor/bhy333 -
ENeuro 2019The ability to recognize and identify a smell is highly dependent on multisensory context and expectation, for example, hearing the name of the odor source. Here, we...
The ability to recognize and identify a smell is highly dependent on multisensory context and expectation, for example, hearing the name of the odor source. Here, we develop a novel auditory-odor association task in rats, wherein the animal learns that a specific auditory tone, when associated with a specific odor, predicts reward (Go signal), whereas the same tone associated with a different odor, or vice versa, is not (No-Go signal). The tone occurs prior to the onset of the odor, allowing physiological analyses of sensory-evoked local field potential (LFP) activity to each stimulus in primary auditory cortex and anterior piriform cortex (aPCX). In trained animals that have acquired the task, both auditory and subsequent olfactory cues activate β band oscillations in both the auditory cortex and PCX, suggesting multisensory integration. Naive animals show no such multisensory responses, suggesting the response is learned. In addition to the learned multisensory evoked responses, functional connectivity between auditory cortex and PCX, as assessed with spectral coherence and phase lag index (PLI), is enhanced. Importantly, both the multi-sensory evoked responses and the functional connectivity are context-dependent. In trained animals, the same auditory stimuli presented in the home cage evoke no responses in auditory cortex or PCX, and functional connectivity between the sensory cortices is reduced. Together, the results demonstrate how learning and context shape the expression of multisensory cortical processing. Given that odor identification impairment is associated with preclinical dementia in humans, the mechanisms suggested here may help develop experimental models to assess effects of neuropathology on behavior.
Topics: Animals; Association Learning; Auditory Cortex; Auditory Perception; Evoked Potentials; Male; Odorants; Olfactory Perception; Piriform Cortex; Rats, Long-Evans; Reward
PubMed: 31362955
DOI: 10.1523/ENEURO.0102-19.2019 -
Neuroscience and Biobehavioral Reviews May 2020Despite a growing body of research devoted to the study of how humans encode environmental patterns, there is still no clear consensus about the nature of the... (Review)
Review
Despite a growing body of research devoted to the study of how humans encode environmental patterns, there is still no clear consensus about the nature of the neurocognitive mechanisms underpinning statistical learning nor what factors constrain or promote its emergence across individuals, species, and learning situations. Based on a review of research examining the roles of input modality and domain, input structure and complexity, attention, neuroanatomical bases, ontogeny, and phylogeny, ten core principles are proposed. Specifically, there exist two sets of neurocognitive mechanisms underlying statistical learning. First, a "suite" of associative-based, automatic, modality-specific learning mechanisms are mediated by the general principle of cortical plasticity, which results in improved processing and perceptual facilitation of encountered stimuli. Second, an attention-dependent system, mediated by the prefrontal cortex and related attentional and working memory networks, can modulate or gate learning and is necessary in order to learn nonadjacent dependencies and to integrate global patterns across time. This theoretical framework helps clarify conflicting research findings and provides the basis for future empirical and theoretical endeavors.
Topics: Association Learning; Attention; Humans; Memory, Short-Term; Nerve Net; Neuronal Plasticity; Prefrontal Cortex; Probability Learning; Serial Learning
PubMed: 32018038
DOI: 10.1016/j.neubiorev.2020.01.032 -
Nature Neuroscience Apr 2015Much of our knowledge of the world depends on learning associations (for example, face-name), for which the hippocampus (HPC) and prefrontal cortex (PFC) are critical....
Much of our knowledge of the world depends on learning associations (for example, face-name), for which the hippocampus (HPC) and prefrontal cortex (PFC) are critical. HPC-PFC interactions have rarely been studied in monkeys, whose cognitive and mnemonic abilities are akin to those of humans. We found functional differences and frequency-specific interactions between HPC and PFC of monkeys learning object pair associations, an animal model of human explicit memory. PFC spiking activity reflected learning in parallel with behavioral performance, whereas HPC neurons reflected feedback about whether trial-and-error guesses were correct or incorrect. Theta-band HPC-PFC synchrony was stronger after errors, was driven primarily by PFC to HPC directional influences and decreased with learning. In contrast, alpha/beta-band synchrony was stronger after correct trials, was driven more by HPC and increased with learning. Rapid object associative learning may occur in PFC, whereas HPC may guide neocortical plasticity by signaling success or failure via oscillatory synchrony in different frequency bands.
Topics: Animals; Association Learning; Behavior, Animal; Brain Waves; Feedback, Physiological; Hippocampus; Macaca mulatta; Prefrontal Cortex; Psychomotor Performance
PubMed: 25706471
DOI: 10.1038/nn.3954 -
Journal of Cognitive Neuroscience Mar 2018Associative learning underlies the formation of new episodic memories. Associative memory improves across development, and this age-related improvement is supported by...
Associative learning underlies the formation of new episodic memories. Associative memory improves across development, and this age-related improvement is supported by the development of the hippocampus and pFC. Recent work, however, additionally suggests a role for visual association cortex in the formation of associative memories. This study investigated the role of category-preferential visual processing regions in associative memory across development using a paired associate learning task in a sample of 56 youths (age 6-19 years). Participants were asked to bind an emotional face with an object while undergoing fMRI scanning. Outside the scanner, participants completed a memory test. We first investigated age-related changes in neural recruitment and found linear age-related increases in activation in lateral occipital cortex and fusiform gyrus, which are involved in visual processing of objects and faces, respectively. Furthermore, greater activation in these visual processing regions was associated with better subsequent memory for pairs over and above the effect of age and of hippocampal and pFC activation on performance. Recruitment of these visual processing regions mediated the association between age and memory performance, over and above the effects of hippocampal activation. Taken together, these findings extend the existing literature to suggest that greater recruitment of category-preferential visual processing regions during encoding of associative memories is a neural mechanism explaining improved memory across development.
Topics: Adolescent; Association Learning; Brain Mapping; Child; Emotions; Facial Recognition; Female; Humans; Magnetic Resonance Imaging; Male; Memory, Episodic; Visual Cortex; Visual Pathways; Young Adult
PubMed: 29064341
DOI: 10.1162/jocn_a_01202 -
Brain Imaging and Behavior Oct 2018In humans, food is considered a powerful primary reinforcer, whereas money is a secondary reinforcer, as it gains a value through learning experience. Here, we aimed to...
In humans, food is considered a powerful primary reinforcer, whereas money is a secondary reinforcer, as it gains a value through learning experience. Here, we aimed to identify the neural regions supporting the processing of food-related reinforcers, relate it to the neural underpinnings of monetary reinforcers, and explore their modulation by metabolic state (hunger vs satiety). Twenty healthy male participants were tested in two experimental sessions, once hungry and once satiated, using functional magnetic resonance imaging. Participants performed an associative learning task, receiving food or monetary rewards (in the form of images) on separate blocks. Irrespective of incentive type, both food and monetary rewards engaged ventral striatum, medial orbitofrontal cortex and amygdala, regions that have been previously associated with reward processing. Food incentives additionally engaged the opercular part of the inferior frontal gyrus and the insula, collectively known as a primary gustatory cortex. Moreover, in response to negative feedback (here, reward omission), robust activation was observed in anterior insula, supplementary motor area and lateral parts of the prefrontal cortex, including middle and inferior frontal gyrus. Furthermore, the interaction between metabolic state and incentive type resulted in supramarginal gyrus (SMG) activity, among other motor and sensory-related regions. Finally, functional connectivity analysis showed correlation in the hungry state between the SMG and mesolimbic regions, including the hippocampus, midbrain and cingulate areas. Also, the interaction between metabolic state and incentive type revealed coupling between SMG and ventral striatum. Whereas general purpose reward-related regions process incentives of different kinds, the current results suggest that the SMG might play a key role in integrating the information related to current metabolic state and available incentive type.
Topics: Adolescent; Adult; Association Learning; Brain; Brain Mapping; Feedback, Psychological; Food; Humans; Hunger; Magnetic Resonance Imaging; Male; Motivation; Reward; Satiation; Visual Perception; Young Adult
PubMed: 29243121
DOI: 10.1007/s11682-017-9811-y -
Neuropsychologia Jun 2019Initial stages of reading acquisition require the learning of letter and speech sound combinations. While the long-term effects of audio-visual learning are rather well...
Initial stages of reading acquisition require the learning of letter and speech sound combinations. While the long-term effects of audio-visual learning are rather well studied, relatively little is known about the short-term learning effects at the brain level. Here we examined the cortical dynamics of short-term learning using magnetoencephalography (MEG) and electroencephalography (EEG) in two experiments that respectively addressed active and passive learning of the association between shown symbols and heard syllables. In experiment 1, learning was based on feedback provided after each trial. The learning of the audio-visual associations was contrasted with items for which the feedback was meaningless. In experiment 2, learning was based on statistical learning through passive exposure to audio-visual stimuli that were consistently presented with each other and contrasted with audio-visual stimuli that were randomly paired with each other. After 5-10 min of training and exposure, learning-related changes emerged in neural activation around 200 and 350 ms in the two experiments. The MEG results showed activity changes at 350 ms in caudal middle frontal cortex and posterior superior temporal sulcus, and at 500 ms in temporo-occipital cortex. Changes in brain activity coincided with a decrease in reaction times and an increase in accuracy scores. Changes in EEG activity were observed starting at the auditory P2 response followed by later changes after 300 ms. The results show that the short-term learning effects emerge rapidly (manifesting in later stages of audio-visual integration processes) and that these effects are modulated by selective attention processes.
Topics: Adult; Association Learning; Cerebral Cortex; Electroencephalography; Evoked Potentials; Evoked Potentials, Auditory; Female; Humans; Magnetoencephalography; Male; Pattern Recognition, Visual; Speech Perception; Young Adult
PubMed: 30930303
DOI: 10.1016/j.neuropsychologia.2019.03.016 -
European Neuropsychopharmacology : the... Jan 2018Cue-associated learning is vital to guiding behaviour for survival. Adolescence represents a key developmental stage for perturbations in cue-related learning, including... (Review)
Review
Cue-associated learning is vital to guiding behaviour for survival. Adolescence represents a key developmental stage for perturbations in cue-related learning, including a characteristic deficit in cue extinction learning. The present review summarizes evidence from animal and human literature that cue extinction is critically mediated by prefrontal dopamine, a system that undergoes dramatic reorganization during adolescence. We propose that extinction learning and memory is governed by a developmentally dynamic balance of dopamine receptors in the prefrontal cortex, which changes across adolescence into adulthood. This is contrary to the previous idea that extinction deficits during adolescence reflect inefficiency in the same neural circuitry as adults. This leads to proposal of the novel theory that cue extinction involves divergent prefrontal dopaminergic mechanisms depending on the age of extinction.
Topics: Animals; Association; Cues; Dopamine; Extinction, Psychological; Fear; Humans; Models, Neurological; Prefrontal Cortex; Sexual Maturation
PubMed: 29174948
DOI: 10.1016/j.euroneuro.2017.11.004 -
NeuroImage Nov 2020Memories are not stored as static engrams, but as dynamic representations affected by processes occurring after initial encoding. Previous studies revealed changes in...
Memories are not stored as static engrams, but as dynamic representations affected by processes occurring after initial encoding. Previous studies revealed changes in activity and mnemonic representations in visual processing areas, parietal lobe, and hippocampus underlying repeated retrieval and suppression. However, these neural changes are usually induced by memory modulation immediately after memory formation. Here, we investigated 27 healthy participants with a two-day functional Magnetic Resonance Imaging study design to probe how established memories are dynamically modulated by retrieval and suppression 24 h after learning. Behaviorally, we demonstrated that established memories can still be strengthened by repeated retrieval. By contrast, repeated suppression had a modest negative effect, and suppression-induced forgetting was associated with individual suppression efficacy. Neurally, we demonstrated item-specific pattern reinstatements in visual processing areas, parietal lobe, and hippocampus. Then, we showed that repeated retrieval reduced activity amplitude in the ventral visual cortex and hippocampus, but enhanced the distinctiveness of activity patterns in the ventral visual cortex and parietal lobe. Critically, reduced activity was associated with enhanced representation of idiosyncratic memory traces in the ventral visual cortex and precuneus. In contrast, repeated memory suppression was associated with reduced lateral prefrontal activity, but relative intact mnemonic representations. Our results replicated most of the neural changes induced by memory retrieval and suppression immediately after learning and extended those findings to established memories after initial consolidation. Active retrieval seems to promote episode-unique mnemonic representations in the neocortex after initial encoding but also consolidation.
Topics: Adolescent; Adult; Association Learning; Brain Mapping; Cerebral Cortex; Cues; Female; Hippocampus; Humans; Image Interpretation, Computer-Assisted; Magnetic Resonance Imaging; Male; Memory Consolidation; Memory, Episodic; Mental Recall; Pattern Recognition, Visual; Spatial Memory; Support Vector Machine; Young Adult
PubMed: 32739553
DOI: 10.1016/j.neuroimage.2020.117213 -
Alzheimer's Research & Therapy Mar 2018Recent evidence derived from functional magnetic resonance imaging (fMRI) studies suggests that functional hubs (i.e., highly connected brain regions) are important for...
BACKGROUND
Recent evidence derived from functional magnetic resonance imaging (fMRI) studies suggests that functional hubs (i.e., highly connected brain regions) are important for mental health. We found recently that global connectivity of a hub in the left frontal cortex (LFC connectivity) is associated with relatively preserved memory abilities and higher levels of protective factors (education, IQ) in normal aging and Alzheimer's disease. These results suggest that LFC connectivity supports reserve capacity, alleviating memory decline. An open question, however, is why LFC connectivity is beneficial and supports memory function in the face of neurodegeneration. We hypothesized that higher LFC connectivity is associated with enhanced efficiency in connected major networks involved in episodic memory. We further hypothesized that higher LFC-related network efficiency predicts higher memory abilities.
METHODS
We assessed fMRI during a face-name association learning task performed by 26 healthy, cognitively normal elderly participants. Using beta-series correlation analysis, we computed task-related LFC connectivity to key memory networks, including the default mode network (DMN) and dorsal attention network (DAN). Network efficiency within the DMN and DAN was estimated by the graph theoretical small-worldness statistic. We applied linear regression analyses to test the association between LFC connectivity with the DMN/DAN and small-worldness of these networks. Mediation analysis was applied to test LFC connectivity to the DMN and DAN as a mediator of the association between education and higher DMN and DAN small-worldness. Last, we tested network small-worldness as a predictor of memory performance.
RESULTS
We found that higher LFC connectivity to the DMN and DAN during successful memory encoding and recognition was associated with higher small-worldness of those networks. Higher task-related LFC connectivity mediated the association between education and higher small-worldness in the DMN and DAN. Further, higher small-worldness of these networks predicted better performance in the memory task.
CONCLUSIONS
The present results suggest that higher education-related LFC connectivity to key memory networks during a memory task is associated with higher network efficiency and thus enhanced reserve of memory abilities in aging.
Topics: Aged; Aged, 80 and over; Aging; Association Learning; Attention; Brain Mapping; Female; Frontal Lobe; Functional Laterality; Humans; Image Processing, Computer-Assisted; Magnetic Resonance Imaging; Male; Middle Aged; Models, Neurological; Neural Pathways; Oxygen; Photic Stimulation
PubMed: 29510747
DOI: 10.1186/s13195-018-0358-y