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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 -
The Journal of Physiology Oct 2014Acetylcholine is a crucial neuromodulator for attention, learning and memory. Release of acetylcholine in primary sensory cortex enhances processing of sensory stimuli,... (Review)
Review
Acetylcholine is a crucial neuromodulator for attention, learning and memory. Release of acetylcholine in primary sensory cortex enhances processing of sensory stimuli, and many in vitro studies have pinpointed cellular mechanisms that could mediate this effect. In contrast, how cholinergic modulation shapes the function of intact circuits during behaviour is only beginning to emerge. Here we review recent data on the recruitment of identified interneuron types in neocortex by cholinergic signalling, obtained with a combination of genetic targeting of cell types, two-photon imaging and optogenetics. These results suggest that acetylcholine release during basal forebrain stimulation, and during physiological recruitment of the basal forebrain, can strongly and rapidly influence the firing of neocortical interneurons. In contrast to the traditional view of neuromodulation as a relatively slow process, cholinergic signalling can thus rapidly convey time-locked information to neocortex about the behavioural state of the animal and the occurrence of salient sensory stimuli. Importantly, these effects strongly depend on interneuron type, and different interneuron types in turn control distinct aspects of circuit function. One prominent effect of phasic acetylcholine release is disinhibition of pyramidal neurons, which can facilitate sensory processing and associative learning.
Topics: Acetylcholine; Animals; Association Learning; Interneurons; Neocortex
PubMed: 24879871
DOI: 10.1113/jphysiol.2014.273862 -
The Journal of Neuroscience : the... Sep 2015Rewards obtained from specific behaviors can and do change across time. To adapt to such conditions, humans need to represent and update associations between behaviors...
Rewards obtained from specific behaviors can and do change across time. To adapt to such conditions, humans need to represent and update associations between behaviors and their outcomes. Much previous work focused on how rewards affect the processing of specific tasks. However, abstract associations between multiple potential behaviors and multiple rewards are an important basis for adaptation as well. In this experiment, we directly investigated which brain areas represent associations between multiple tasks and rewards, using time-resolved multivariate pattern analysis of functional magnetic resonance imaging data. Importantly, we were able to dissociate neural signals reflecting task-reward associations from those related to task preparation and reward expectation processes, variables that were often correlated in previous research. We hypothesized that brain regions involved in processing tasks and/or rewards will be involved in processing associations between them. Candidate areas included the dorsal anterior cingulate cortex, which is involved in associating simple actions and rewards, and the parietal cortex, which has been shown to represent task rules and action values. Our results indicate that local spatial activation patterns in the inferior parietal cortex indeed represent task-reward associations. Interestingly, the parietal cortex flexibly changes its content of representation within trials. It first represents task-reward associations, later switching to process tasks and rewards directly. These findings highlight the importance of the inferior parietal cortex in associating behaviors with their outcomes and further show that it can flexibly reconfigure its function within single trials. Significance statement: Rewards obtained from specific behaviors rarely remain constant over time. To adapt to changing conditions, humans need to continuously update and represent the current association between behavior and its outcomes. However, little is known about the neural representation of behavior-outcome associations. Here, we used multivariate pattern analysis of functional magnetic resonance imaging data to investigate the neural correlates of such associations. Our results demonstrate that the parietal cortex plays a central role in representing associations between multiple behaviors and their outcomes. They further highlight the flexibility of the parietal cortex, because we find it to adapt its function to changing task demands within trials on relatively short timescales.
Topics: Adult; Association Learning; Female; Humans; Male; Parietal Lobe; Reward
PubMed: 26354905
DOI: 10.1523/JNEUROSCI.4882-14.2015 -
The Journal of Neuroscience : the... Nov 2013The mesocorticolimbic system, consisting, at its core, of the ventral tegmental area, the nucleus accumbens, and medial prefrontal cortex, has historically been... (Review)
Review
The mesocorticolimbic system, consisting, at its core, of the ventral tegmental area, the nucleus accumbens, and medial prefrontal cortex, has historically been investigated primarily for its role in positively motivated behaviors and reinforcement learning, and its dysfunction in addiction, schizophrenia, depression, and other mood disorders. Recently, researchers have undertaken a more comprehensive analysis of this system, including its role in not only reward but also punishment, as well as in both positive and negative reinforcement. This focus has been facilitated by new anatomical, physiological, and behavioral approaches to delineate functional circuits underlying behaviors and to determine how this system flexibly encodes and responds to positive and negative states and events, beyond simple associative learning. This review is a summary of topics covered in a mini-symposium at the 2013 Society for Neuroscience annual meeting.
Topics: Animals; Association Learning; Dopamine; Dopaminergic Neurons; Nerve Net; Nucleus Accumbens; Prefrontal Cortex; Reward; Ventral Tegmental Area
PubMed: 24198347
DOI: 10.1523/JNEUROSCI.3250-13.2013 -
Neuron Dec 1998
Review
Topics: Animals; Association Learning; Brain; Cerebral Cortex; Models, Neurological; Nerve Net; Perception; Prefrontal Cortex; Primates
PubMed: 9883712
DOI: 10.1016/s0896-6273(00)80638-8 -
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 -
Current Biology : CB Jan 2015The frontal association cortex (FrA) is implicated in higher brain function. Aberrant FrA activity is likely to be involved in dementia pathology. However, the...
The frontal association cortex (FrA) is implicated in higher brain function. Aberrant FrA activity is likely to be involved in dementia pathology. However, the functional circuits both within the FrA and with other regions are unclear. A recent study showed that inactivation of the FrA impairs memory consolidation of an auditory fear conditioning in young mice. In addition, dendritic spine remodeling of FrA neurons is sensitive to paired sensory stimuli that produce associative memory. These findings suggest that the FrA is engaged in neural processes critical to associative learning. Here we characterize stimulus integration in the mouse FrA during associative learning. We experimentally separated contextual fear conditioning into context exposure and shock, and found that memory formation requires protein synthesis associated with both context exposure and shock in the FrA. Both context exposure and shock trigger Arc, an activity-dependent immediate-early gene, expression in the FrA, and a subset of FrA neurons was dually activated by both stimuli. In addition, we found that the FrA receives projections from the perirhinal (PRh) and insular (IC) cortices and basolateral amygdala (BLA), which are implicated in context and shock encoding. PRh and IC neurons projecting to the FrA were activated by context exposure and shock, respectively. Arc expression in the FrA associated with context exposure and shock depended on PRh activity and both IC and BLA activities, respectively. These findings indicate that the FrA is engaged in stimulus integration and contributes to memory formation in associative learning.
Topics: Animals; Association Learning; Conditioning, Psychological; Fear; Frontal Lobe; Male; Mice, Inbred C57BL; Neurons; Protein Biosynthesis
PubMed: 25496961
DOI: 10.1016/j.cub.2014.10.078 -
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 -
The Journal of Neuroscience : the... Feb 2022Acquiring new memories is a multistage process. Numerous studies have convincingly demonstrated that initially acquired memories are labile and are stabilized only by...
Acquiring new memories is a multistage process. Numerous studies have convincingly demonstrated that initially acquired memories are labile and are stabilized only by later consolidation processes. These multiple phases of memory formation are known to involve modification of both cellular excitability and synaptic connectivity, which in turn change neuronal activity at both the single neuron and ensemble levels. However, the specific mapping between the known phases of memory and the changes in neuronal activity at different organizational levels-the single-neuron, population representations, and ensemble-state dynamics-remains unknown. Here we address this issue in the context of conditioned taste aversion learning by continuously tracking gustatory cortex neuronal taste responses in alert male and female rats during the 24 h following a taste-malaise pairing. We found that the progression of activity changes depends on the neuronal organizational level: whereas the population response changed continuously, the population mean response amplitude and the number of taste-responsive neurons only increased during the acquisition and consolidation phases. In addition, the known quickening of the ensemble-state dynamics associated with the faster rejection of harmful foods appeared only after consolidation. Overall, these results demonstrate how complex dynamics in the different representational levels of cortical activity underlie the formation and stabilization of memory within the cortex. Memory formation is a multiphased process; early acquired memories are labile and consolidate to their stable forms over hours and days. The progression of memory is assumed to be supported by changes in neuronal activity, but the mapping between memory phases and neuronal activity changes remains elusive. Here we tracked cortical neuronal activity over 24 h as rats acquired and consolidated a taste-malaise association memory, and found specific differences between the progression at the single-neuron and populations levels. These results demonstrate how balanced changes on the single-neuron level lead to changes in the network-level representation and dynamics required for the stabilization of memories.
Topics: Animals; Association Learning; Female; Male; Memory Consolidation; Neurons; Rats; Rats, Long-Evans; Sensorimotor Cortex; Taste Perception
PubMed: 34916257
DOI: 10.1523/JNEUROSCI.1599-21.2021 -
The Journal of Neuroscience : the... Aug 2018Perception can be cast as a process of inference, in which bottom-up signals are combined with top-down predictions in sensory systems. In line with this, neural...
Perception can be cast as a process of inference, in which bottom-up signals are combined with top-down predictions in sensory systems. In line with this, neural activity in sensory cortex is strongly modulated by prior expectations. Such top-down predictions often arise from cross-modal associations, such as when a sound (e.g., bell or bark) leads to an expectation of the visual appearance of the corresponding object (e.g., bicycle or dog). We hypothesized that the hippocampus, which rapidly learns arbitrary relationships between stimuli over space and time, may be involved in forming such associative predictions. We exposed male and female human participants to auditory cues predicting visual shapes, while measuring high-resolution fMRI signals in visual cortex and the hippocampus. Using multivariate reconstruction methods, we discovered a dissociation between these regions: representations in visual cortex were dominated by whichever shape was presented, whereas representations in the hippocampus reflected only which shape was predicted by the cue. The strength of hippocampal predictions correlated across participants with the amount of expectation-related facilitation in visual cortex. These findings help bridge the gap between memory and sensory systems in the human brain. The way we perceive the world is to a great extent determined by our prior knowledge. Despite this intimate link between perception and memory, these two aspects of cognition have mostly been studied in isolation. Here we investigate their interaction by asking how memory systems that encode and retrieve associations can inform perception. We find that upon hearing a familiar auditory cue, the hippocampus represents visual information that had previously co-occurred with the cue, even when this expectation differs from what is currently visible. Furthermore, the strength of this hippocampal expectation correlates with facilitation of perceptual processing in visual cortex. These findings help bridge the gap between memory and sensory systems in the human brain.
Topics: Adult; Association; Association Learning; Cues; Female; Form Perception; Hippocampus; Humans; Magnetic Resonance Imaging; Male; Neuroimaging; Pattern Recognition, Physiological; Visual Cortex
PubMed: 29986875
DOI: 10.1523/JNEUROSCI.0163-18.2018