A Neural Correlate of Working Memory in the Monkey Primary Visual Cortex

Supèr, Hans; Spekreijse, H.; Lamme, Victor A. F.

doi:10.1126/science.1060496

Cited by 278 publications

(184 citation statements)

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“…For example, it is possible that those primary areas not only represent modalityspecific sensory information while a stimulus is presented, but also are able to maintain some of that information ''on line'' during the working memory period of a discrimination task, and perhaps even participate in the subsequent decision-making steps. For instance, there are several reports suggesting that primary sensory cortices are involved to some degree in working memory tasks (34)(35)(36). Furthermore, a recent study has shown that, in addition to representing acoustic features, responses in A1 and R auditory fields may serve to encode some cognitive task elements associated with auditory processing (29), which also seems consistent with the idea that auditory cortex becomes selective to other sensory modalities when these are associated with auditory processing during action selection (29).…”

Section: Discussionsupporting

confidence: 62%

Neural codes for perceptual discrimination of acoustic flutter in the primate auditory cortex

Lemus

Hernandez

Romo

2009

Proc. Natl. Acad. Sci. U.S.A.

106

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We recorded from single neurons of the primary auditory cortex (A1), while trained monkeys reported a decision based on the comparison of 2 acoustic flutter stimuli. Crucially, to form the decision, monkeys had to compare the second stimulus rate to the memory trace of the first stimulus rate. We found that the responses of A1 neurons encode stimulus rates both through their periodicity and through their firing rates during the stimulation periods, but not during the working memory and decision components of this task. Neurometric thresholds based on firing rate were very similar to the monkey's discrimination thresholds, whereas neurometric thresholds based on periodicity were lower than the experimental thresholds. Thus, an observer could solve this task with a precision similar to that of the monkey based only on the firing rates evoked by the stimuli. These results suggest that the A1 is exclusively associated with the sensory and not with the cognitive components of this task.decision making ͉ monkeys ͉ working memory ͉ psychophysics ͉ neurophysiology T he problem of how sensory experiences arise from activity in the brain has stimulated a large amount of research in neuroscience (1, 2). A major component of this problem involves understanding how the brain represents sensory features-that is, what attributes of the neural responses evoked by a stimulus are meaningful for sensation, perception, memory, and decisionmaking? To confront these issues unambiguously, experimental methods should conform to 2 essential conditions: first, the sensory stimulus must be under precise, quantitative control, and second, the subject's psychophysical responses should be well controlled and quantitatively measured. Most experimental paradigms meeting these standards have involved vision (1, 3) and somatosensation (2, 4). In comparison, the amount of research about audition using this approach is scant (5). Most of the studies in the auditory cortex and related areas have described the response properties of neurons to auditory scenes in anesthetized and awake animals, and how these are affected by different task conditions (5-21). But how the neural representations of acoustic stimuli are related to perception, memory and decision making is not known.We addressed this problem by recording the activity of single neurons in the primary auditory cortex (A1), while trained monkeys discriminated the difference in rate of 2 acoustic flutter stimuli (range of 4-40 Hz). The sensation of acoustic flutter is produced by slow repetition of an acoustic stimulus (11). The rate of the acoustic flutter is determined by the interval between the acoustic stimuli (pulse trains). In the acoustic flutter discrimination task, monkeys report whether the second stimulus rate (f2) is higher or lower than the first stimulus rate (f1). This cognitive operation requires that subjects compare information of f2 with a stored trace of f1 to form a decision, that is, whether f2 Ͼ f1 or f2 Ͻ f1, and to report their perceptual evaluation after a short, fix...

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Section: Discussionsupporting

confidence: 62%

Neural codes for perceptual discrimination of acoustic flutter in the primate auditory cortex

Lemus

Hernandez

Romo

2009

Proc. Natl. Acad. Sci. U.S.A.

106

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Section: Discussionmentioning

confidence: 99%

“…Although the functional significance of NT changes is not clear, it might be of relevance that two other neuropeptides interacting with the dopaminergic system, Calcitonin gene-related peptide (CGRP) and substance P are also decreased by risperidone and unaffected by haloperidol (Gruber and Mathé 1999). In view of interactions between working memory, a prefrontal cortex task, and visual attention tasks, localized in the occipital cortex (de Fockert et al 2001;Supèr et al 2001) and the observations that these processes are deranged in schizophrenia, selective effects of risperidone on NT, CGRP and substance P might constitute biological correlates of its beneficial effects on cognitive processes.As far as the microdialysis results, haloperidol and the higher dose of risperidone decreased basal extracellular NT-LI levels in the VSTR. These findings are in line with results showing decreased extracellular NT-LI concentrations in the nucleus accumbens and the caudate putamen following treatment with eticlopride, a DA-D 2 receptor antagonist (Wagstaff et al 1996a).…”

mentioning

confidence: 99%

Effects of Haloperidol and Risperidone on Neurotensin Levels in Brain Regions and Neurotensin Efflux in the Ventral Striatum of the Rat

Gruber

Nomikos

Mathé

2002

Neuropsychopharmacology

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Neurotensin (NT) may play a role in the pathophysiology of schizophrenia and in the mechanism of action of antipsychotic drugs. Here we studied the effects of a 30-day regimen of haloperidol (1.15 mg/100 g food) and risperidone (1.15 and 2.3 mg/100 g food) on NT-like immunoreactivity (-LI) levels in brain tissue and NT-LI efflux in the ventral striatum (VSTR) of the rat. Haloperidol, but not risperidone, increased NT-LI levels in the striatum. In the occipital cortex, risperidone, but not haloperidol, decreased levels of NT-LI. In the hippocampus and the frontal cortex both haloperidol and risperidone (the higher dose) increased NT-LI levels. In the VSTR, haloperidol and risperidone (the higher dose) decreased NT-LI efflux and abolished the stimulatory effect of d-amphetamine (1.5 mg/kg, s.c.). Thus, changes in NT occur in response toNeurotensin (NT) is a 13-amino acid peptide originally isolated from hypothalamus (Carraway and Leeman 1973). Several anatomical, behavioral and pharmacological studies have demonstrated an interaction between NT and dopamine (DA) in the central nervous system (CNS). For example, high levels of NT and its binding sites have been found in both the cell body regions, i.e. the substantia nigra pars compacta (SN) and the ventral tegmental area (VTA), as well as the major projection areas of the ascending dopaminergic pathways, i.e. the striatum and the nucleus accumbens (Kasckow and Nemeroff 1991;Lambert et al. 1995; Quirion 1983). Within both the VTA and the SN, NT immunoreactive fibers are found in close proximity to DA cell bodies (Hökfelt et al. 1984); within the VTA, NT is colocalized with DA (Hökfelt et al. 1984;Kalivas 1993), while in the striatal complex, the majority of the NT binding sites in rat are located on DA terminals (Cadet et al. 1991). There exists substantial pharmacological evidence showing that NT is involved in the regulation of DA neurotransmission. For example, local perfusion with NT dose-dependently increases striatal extracellular DA levels without affecting DA metabolite levels and modifies the inhibitory effects of DA-D 1 and DA-D 2 receptor agonists on striatal DA release (Fuxe et al. 1992). In contrast to the striatum, in the nucleus accumbens direct infu- NO . 5 sion of NT does not affect extracellular DA levels, but increases extracellular levels of the DA metabolite homovanillic acid (Chapman et al. 1992). Microinjection of NT into the VTA, produces a dose-dependent in vivo DA release in the nucleus accumbens and also causes a dose-dependent circling behavior (Steinberg et al. 1995). Moreover, blockade of NT receptors by the NT receptor antagonist SR 48692 decreases basal extracellular levels of DA and its metabolites in the nucleus accumbens, suggesting that NT modulates the mesolimbic DA system (Azzi et al. 1998). Neurotensin has also been shown to mimic the effects of neuroleptic drugs in behavioral models of antipsychotic drug action. Thus, centrally injected NT antagonizes psychostimulant-induced locomotor hyperactivity (Ervin et al. 1981;Joli...

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“…Specifically, we show that alpha-band oscillations can be used to track when a memory representation changes its state from a passive long-term memory to an active working memory (44). Given the evidence that the similar patterns of neural activity represent perceptual inputs and maintain those representations in working memory (45)(46)(47), we propose that the alpha-band activity we measured indicates a shift to the same active state by the neurons that store longterm memories.…”

Section: Discussionmentioning

confidence: 99%

Visual working memory buffers information retrieved from visual long-term memory

Fukuda

Woodman

2017

Proc. Natl. Acad. Sci. U.S.A.

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Human memory is thought to consist of long-term storage and shortterm storage mechanisms, the latter known as working memory. Although it has long been assumed that information retrieved from long-term memory is represented in working memory, we lack neural evidence for this and need neural measures that allow us to watch this retrieval into working memory unfold with high temporal resolution. Here, we show that human electrophysiology can be used to track information as it is brought back into working memory during retrieval from long-term memory. Specifically, we found that the retrieval of information from long-term memory was limited to just a few simple objects' worth of information at once, and elicited a pattern of neurophysiological activity similar to that observed when people encode new information into working memory. Our findings suggest that working memory is where information is buffered when being retrieved from long-term memory and reconcile current theories of memory retrieval with classic notions about the memory mechanisms involved.visual working memory | visual long-term memory retrieval | EEG H umans are capable of storing an essentially limitless amount of information in long-term memory and can remember specific pieces of information when needed to guide behavior. For over a century, researchers have proposed that, when humans retrieve information from long-term memory, we do this by bringing the information back into working memory (1-3). This has become so engrained in the dogma regarding how human memory works that retrieving information from long-term memory into working memory is described in introductory textbooks (e.g., refs. 4 and 5). However, although there is behavioral evidence in line with the notion that information retrieved from long-term memory is brought back into working memory (ref. 6; see ref. 7 for a review of additional classic evidence; refs. 8-10), a direct demonstration that this is occurring in brain is needed. If we were able to track this cognitive process, we could use it to understand the fine-grained dynamics of memory retrieval.In the present study, we took advantage of the fact that encoding new sensory information into working memory is capacity limited (11-16). Neuroscientific studies have established that the encoding of a subset of the available visual information into working memory can be measured by frequency-specific oscillations of subjects' electroencephalograms (EEGs) (17)(18)(19)(20). Specifically, the magnitude of suppression of alpha-band oscillations (8-13 Hz) measured across parieto-occipital channels as new information is held in working memory changes as additional information is loaded into working memory and hits an asymptote at a subject's working-memory capacity estimated from behavioral performance. We chose this neural correlate of working memory over other correlates (e.g., the contralateral delay activity in ref. 12) because it allowed the estimation of working-memory load without necessitating the presentation of to-be-ignored dis...

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A Neural Correlate of Working Memory in the Monkey Primary Visual Cortex

Abstract: A neural correlate of working memory in the monkey primary visual cortex Lamme, V.A.F.; Suphr, H.; Spekreijse, H.

Cited by 278 publications

References 11 publications

Neural codes for perceptual discrimination of acoustic flutter in the primate auditory cortex

Neural codes for perceptual discrimination of acoustic flutter in the primate auditory cortex

Effects of Haloperidol and Risperidone on Neurotensin Levels in Brain Regions and Neurotensin Efflux in the Ventral Striatum of the Rat

Visual working memory buffers information retrieved from visual long-term memory

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