Rapid Association Learning in the Primate Prefrontal Cortex in the Absence of Behavioral Reversals (original) (raw)
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Neural activity in the primate prefrontal cortex during associative learning
Neuron, 1998
CITATIONS 353 READS 43 3 authors: Some of the authors of this publication are also working on these related projects: Synchrony of beta oscillations in the frontoparietal network View project Category representations in parietal and prefrontal cortex on different levels of category abstractness
It is thought that the ability to learn and follow abstract rules relies on intact prefrontal regions including the lateral prefrontal cortex (LPFC) and the orbitofrontal cortex (OFC). To learn more about the differences between LPFC and OFC in rule learning, we tested monkeys with bilateral removals of either LPFC or OFC on a rapidly learned task requiring the formation of the abstract concept of same/different. While monkeys with OFC removals were significantly slower than controls at both acquiring and reversing the concept-based rule, monkeys with LPFC removals were not impaired in acquiring the task, but were significantly slower at rule reversal. Neither group was impaired in the acquisition or reversal of a delayed visual cue-outcome association task without a concept-based rule. These results suggest that OFC is essential for the implementation of a concept-based rule, whereas LPFC seems essential for its modification once established.
Prefrontal-inferotemporal interaction is not always necessary for reversal learning.
Prefrontal cortex (PFC) is thought to have a wide-ranging role in cognition, often described as executive function or behavioral inhibition. A specific example of such a role is the inhibition of representations in more posterior regions of cortex in a "top-down" manner, a function thought to be tested by reversal learning tasks. The direct action of PFC on posterior regions can be directly tested by disconnecting PFC from the region in question. We tested whether PFC directly inhibits visual object representations in inferotemporal cortex (IT) during reversal learning by studying the effect, in macaque monkeys, of disconnecting PFC from IT by crossed unilateral ablations. We tested two visual object reversal learning tasks, namely serial and concurrent reversal learning. We found that the disconnection severely impairs serial reversal learning but leaves concurrent reversal learning completely intact. Thus, PFC cannot be said to always have direct inhibitory control over visual object representations in reversal learning. Furthermore, our results cannot be explained by generalized theories of PFC function such as executive function and behavioral inhibition, because those theories do not make predictions that differentiate different forms of reversal learning. The results do, however, support our proposal, based on other experimental evidence from macaque monkeys, that PFC has a highly specific role in the representation of temporally complex events.
Neural Correlates of Learning in the Prefrontal Cortex of the Monkey: A Predictive Model
Cerebral Cortex, 1995
The principles underlying the organization and operation of the prefrontal cortex have been addressed by neural network modeling. The involvement of the prefrontal cortex in the temporal organization of behavior can be defined by processing units that switch between two stable states of activity (bistable behavior) in response to synaptic inputs. Long-term representation of programs requiring short-term memory can result from activity-dependent modifications of the synaptic transmission controlling the bistable behavior. After learning, the sustained activity of a given neuron represents the selective memorization of a past event the selective anticipation of a future event, and the predictability of reinforcement A simulated neural network illustrates the abilities of the model (1) to learn, via a natural step-by-step training protocol, the paradigmatic task (delayed response) used for testing prefrontal neurons in primates, (2) to display the same categories of neuronal activities, and (3) to predict how they change during learning. In agreement with experimental data, two main types of activity contribute to the adaptive properties of the network. The first is transient activity time-locked to events of the task and its profile remains constant during successive training stages. The second is sustained activity that undergoes nonmonotonic changes with changes in reward contingency that occur during the transition between stages.
Frequency-specific hippocampal-prefrontal interactions during associative learning
Nature neuroscience, 2015
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...
Trial outcome and associative learning signals in the monkey hippocampus
Neuron, 2009
In tasks of associative learning, animals establish new links between unrelated items by using information about trial outcome to strengthen correct/rewarded associations and modify incorrect/unrewarded ones. To study how hippocampal neurons convey information about reward and trial outcome during new associative learning, we recorded hippocampal neurons as monkeys learned novel object-place associations. A large population of hippocampal neurons (50%) signaled trial outcome by differentiating between correct and error trials during the period after the behavioral response. About half these cells increased their activity following correct trials (correct up cells) while the remaining half fired more following error trials (error up cells). Moreover, correct up cells, but not error up cells, conveyed information about learning by increasing their stimulus-selective response properties with behavioral learning. These findings suggest that information about successful trial outcome con...
Integrating associative learning signals across the brain
Hippocampus, 2007
Associative learning is defined as the ability to link arbitrary stimuli or actions together in memory. The neural correlates of this fundamental form of plasticity were first described in the hippocampus during delay eye blink conditioning and have since been examined using a variety of tasks in both rats and monkeys. In monkeys, the neural correlates of associative learning have been studied using conditional motor learning tasks where animals learn to associate particular visual stimuli with particular motor responses (i.e., touch left or touch right). Similar tasks have also been used to examine learning-related plasticity in motor-related areas throughout the frontal lobe and striatum. Here, we review the patterns of learning-related activity seen in these diverse brain areas during conditional motor learning. While each of these areas exhibits strong associative learning signals, the differential patterns and time courses of these signals provides insight into the unique contribution of each area to associative learning. V
Specialisation within the prefrontal cortex: the ventral prefrontal cortex and associative learning
Experimental Brain Research, 2000
This paper provides evidence that the ventral prefrontal cortex plays a role in the learning of tasks in which subjects must learn to associate visual cues and responses. Imaging with both positron-emission tomography (PET) and functional magnetic-resonance imaging (fMRI) reveals learning-related increases in activity when normal subjects learn visual associative tasks. Evidence is also presented from an event-related fMRI study that activity in this area is time-locked both to the presentation of the visual stimuli and also to the time of the motor response. Finally, it is shown in a study of monkeys that removal of the ventral prefrontal area 12 (including 45 A) impairs the ability of monkeys to relearn a visual associative task (visual matching), even though there were no demands on working memory. It is, therefore, proposed that the ventral prefrontal cortex constitutes part of the circuitry via which associations are formed between visual cues and the actions or choices that they specify. On the basis of the existing anatomical and electrophysiological data, it is argued that the prefrontal cortex is the only area that can represent cues, responses and outcomes.
Rapid Plasticity in the Prefrontal Cortex during Affective Associative Learning
PLoS ONE, 2014
MultiCS conditioning is an affective associative learning paradigm, in which affective categories consist of many similar and complex stimuli. Comparing visual processing before and after learning, recent MultiCS conditioning studies using timesensitive magnetoencephalography (MEG) revealed enhanced activation of prefrontal cortex (PFC) regions towards emotionally paired versus neutral stimuli already during short-latency processing stages (i.e., 50 to 80 ms after stimulus onset). The present study aimed at showing that this rapid differential activation develops as a function of the acquisition and not the extinction of the emotional meaning associated with affectively paired stimuli. MEG data of a MultiCS conditioning study were analyzed with respect to rapid changes in PFC activation towards aversively (electric shock) paired and unpaired faces that occurred during the learning of stimulus-reinforcer contingencies. Analyses revealed an increased PFC activation towards paired stimuli during 50 to 80 ms already during the acquisition of contingencies, which emerged after a single pairing with the electric shock. Corresponding changes in stimulus valence could be observed in ratings of hedonic valence, although participants did not seem to be aware of contingencies. These results suggest rapid formation and access of emotional stimulus meaning in the PFC as well as a great capacity for adaptive and highly resolving learning in the brain under challenging circumstances. Citation: Rehbein MA, Steinberg C, Wessing I, Pastor MC, Zwitserlood P, et al. (2014) Rapid Plasticity in the Prefrontal Cortex during Affective Associative Learning. PLoS ONE 9(10): e110720.