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Working memory in primate sensory systems

Nature Reviews Neuroscience volume 6, pages 97–107 (2005)Cite this article

An Erratum to this article was published on 01 March 2005

Key Points

  • Psychophysical, physiological and imaging studies of sensory working memory support the idea that elemental sensory dimensions are represented by distinct memory systems that are likely to include the same cortical areas as those involved in encoding stimulus features.

  • In visual psychophysics, this idea is supported by the differences in the length of time for which specific stimulus features are retained, and by studies that use a 'memory masking' approach in which an interaction between an interference stimulus during the memory delay and the preceding stimulus reveals the nature of the remembered stimulus. Memory masking is most effective early in the delay and its effect is specific to the stimulus attributes that are retained. Studies of memory for motion show that the remembered stimuli are spatially localized, indicating the involvement of areas with fairly precise retinotopy, and also show that the spatial scale of the mechanism that underlies performance matches the receptive field size of cortical area MT. Other studies also indicate a separate representation in memory of simple stimulus dimensions such as spatial frequency, orientation and speed.

  • Single-cell recordings in monkeys and imaging studies in humans also reveal memory-related activity in regions of visual cortex that are known to process various attributes of visual stimuli (for example, areas IT, V4 and MT). Lesions of areas MT/MST in monkeys and of analogous regions in humans also produce memory-related deficits in motion discrimination. The involvement of visual cortical areas in retention of visual information is also supported by microstimulation experiments in monkeys and transcranial magnetic stimulation (TMS) in humans.

  • Psychophysical studies of tactile working memory show robust and selective retention of tactile signals, implicating the involvement of the regions that process these signals. Physiological recordings reveal memory-related delay activity at the earliest stages of processing of tactile information in S1 for texture and in S2 for vibration discrimination. Imaging studies also show activation of somatosensory regions in cortex during working memory tasks, and TMS applied to S1 during the delay in the vibration discrimination task disrupted performance.

  • Psychophysical studies of auditory working memory indicate that elementary dimensions, such as frequency, intensity and sound location, are stored by separate modules. Single-cell recordings in primary auditory cortex during the memory delay show activity that carries information about the remembered tone frequency. The involvement of auditory cortex in working memory for sound is also supported by magnetoencephalography, imaging and lesion studies in humans.

  • This review provides evidence for participation of sensory cortical areas in the circuitry that temporarily stores sensory information. However, the precise nature of this participation is still unclear. The use of quantitative sensory psychophysics in conjunction with recording and imaging studies will bring us closer to an understanding of how the brain deals with sensory storage.

Abstract

Sensory working memory consists of the short-term storage of sensory stimuli to guide behaviour. There is increasing evidence that elemental sensory dimensions — such as object motion in the visual system or the frequency of a sound in the auditory system — are stored by segregated feature-selective systems that include not only the prefrontal and parietal cortex, but also areas of sensory cortex that carry out relatively early stages of processing. These circuits seem to have a dual function: precise sensory encoding and short-term storage of this information. New results provide insights into how activity in these circuits represents the remembered sensory stimuli.

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Figure 1: Visual working memory for selected stimulus attributes.
Figure 2: Visual working memory for stimulus direction.
Figure 3: Directional signals in area MT during the memory delay.
Figure 4: Effect of MT/MST lesions on discrimination and memory of the direction of complex motion.
Figure 5: Sensory working memory in patients with focal brain lesions.
Figure 6: Effect of electrical microstimulation of area MT on memory for motion.

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Acknowledgements

T. Pasternak was supported by a grant from the National Eye Institute and, in part, a grant to the Center for Visual Science. M. Greenlee acknowledges financial support from the German Research Foundation. We thank Gregor Rainer for comments on the early version of the manuscript.

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Authors and Affiliations

  1. Departments of Neurobiology & Anatomy, Brain & Cognitive Science and Center for Visual Science, Box 603, University of Rochester, Rochester, 14642, New York, USA

    Tatiana Pasternak

  2. Institute for Experimental Psychology, University of Regensburg, Regensburg, D-93050, Germany

    Mark W. Greenlee

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  1. Tatiana Pasternak
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  2. Mark W. Greenlee
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Correspondence to Tatiana Pasternak.

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FURTHER INFORMATION

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Glossary

VENTRAL AND DORSAL VISUAL STREAMS

Visual information coming from V1 is processed in two interconnected but partly dissociable visual pathways, a 'ventral' pathway extending into the temporal lobe, which is thought to be primarily involved in visual object recognition, and a 'dorsal' pathway extending into the parietal lobes, which are thought to be more involved in extracting information about 'where' an object is or 'how' to execute visually guided action towards it.

ROC

(Receiver operating characteristic). ROC analysis, introduced in signal detection theory, is often used to evaluate the results of a detection task with weak signals. A ROC curve is generated by plotting the probability of true positives (hits) against the probability of false positives (false alarms) for a binary classifier system as its criterion is varied. In neurophysiology, it is used to test whether an ideal observer could reliably identify a given stimulus (such as direction of stimulus motion) or a behaviour based on a neural response (such as firing rate).

N-BACK TASKS

The subject is presented with a series of stimuli and is required to respond when the stimulus on the current trial matches that presented n trials ago. The memory load can be increased by increasing n. The subject has a dual task: to encode the current stimulus and to compare it with that presented on the n-to-last trial.

DELAYED MATCHING-TO-SAMPLE TASKS

Presentation of a stimulus is followed by a delay, after which a choice is offered. In matching tasks, the original stimulus that was presented must be chosen; in non-matching tasks, a new stimulus must be selected. With small stimulus sets, the stimuli are frequently repeated and become highly familiar. So, such tasks are most readily solved by short-term or working memory rather than by long-term memory. In the original version of this task, trained animals or instructed volunteers report whether two stimuli separated by a memory delay are the same or different.

TRANSCRANIAL MAGNETIC STIMULATION

A technique that is used to induce a transient interruption of normal activity in a relatively restricted area of the brain. It is based on the generation of a strong magnetic field near the area of interest, which, if changed rapidly enough, will induce an electric field that is sufficient to stimulate neurons.

PRIMING

The facilitation of recognition, reproduction or biases in the selection of stimuli that have recently been perceived.

MAGNETOENCEPHALOGRAPHY

A non-invasive technique that allows the detection of the changing magnetic fields that are associated with brain activity. As the magnetic fields of the brain are weak, extremely sensitive magnetic detectors known as superconducting quantum interference devices — which work at very low, superconducting temperatures (−269 °C) — are used to pick up the signal.

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Pasternak, T., Greenlee, M. Working memory in primate sensory systems. Nat Rev Neurosci 6, 97–107 (2005). https://doi.org/10.1038/nrn1603

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