Neural Dynamics in Inferior Temporal Cortex during a Visual Working Memory Task

Department of Neuroscience, Brown University, Providence, Rhode Island 02912, USA.
The Journal of Neuroscience : The Official Journal of the Society for Neuroscience (Impact Factor: 6.34). 05/2009; 29(17):5494-507. DOI: 10.1523/JNEUROSCI.5785-08.2009
Source: PubMed

ABSTRACT Intelligent organisms are capable of tracking objects even when they temporarily disappear from sight, a cognitive capacity commonly referred to as visual working memory (VWM). The neural basis of VWM has been the subject of significant scientific debate, with recent work focusing on the relative roles of posterior visual areas, such as the inferior temporal cortex (ITC), and the prefrontal cortex. Here we reexamined the contribution of ITC to VWM by recording from highly selective individual ITC neurons as monkeys engaged in multiple versions of an occlusion-based memory task. As expected, we found strong evidence for a role of ITC in stimulus encoding. We also found that almost half of these selective cells showed stimulus-selective delay period modulation, with a small but significant fraction exhibiting differential responses even in the presence of simultaneously visible interfering information. When we combined the informational content of multiple neurons, we found that the accuracy with which we could decode memory content increased drastically. The memory epoch analyses suggest that behaviorally relevant visual memories were reinstated in ITC. Furthermore, we observed a population-wide enhancement of neuronal response to a match stimulus compared with the same stimulus presented as a nonmatch. The single-cell enhancement preceded any match effects identified in the local field potential, leading us to speculate that enhancement is the result of neural processing local to ITC. Moreover, match enhancement was only later followed by the more commonly observed match suppression. Altogether, the data support the hypothesis that, when a stimulus is held in memory, ITC neurons are actively biased in favor of task-relevant visual representations and that this bias can immediately impact subsequent recognition events.

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    • "This decrease is accompanied by a complementary increase in inferotemporal sources. The parietal lobes are involved in voluntary selection of attention (Posner et al., 1984; Corbetta et al., 2000), while inferotemporal cortex is associated with high-level stimulus categorization and taskrelevant visual representation (Schendan and Stern, 2008; Woloszyn and Sheinberg, 2009). Thus, the observed effects suggest an adaptive increase in the precision of – or confidence in – high-level expectations that provide top-down predictions. "
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    ABSTRACT: This paper tests the hypothesis that patients with schizophrenia have a deficit in selectively attending to predictable events. We used dynamic causal modeling (DCM) of electrophysiological responses - to predictable and unpredictable visual targets - to quantify the effective connectivity within and between cortical sources in the visual hierarchy in 25 schizophrenia patients and 25 age-matched controls. We found evidence for marked differences between normal subjects and schizophrenia patients in the strength of extrinsic backward connections from higher hierarchical levels to lower levels within the visual system. In addition, we show that not only do schizophrenia subjects have abnormal connectivity but also that they fail to adjust or optimize this connectivity when events can be predicted. Thus, the differential intrinsic recurrent connectivity observed during processing of predictable versus unpredictable targets was markedly attenuated in schizophrenia patients compared with controls, suggesting a failure to modulate the sensitivity of neurons responsible for passing sensory information of prediction errors up the visual cortical hierarchy. The findings support the proposed role of abnormal connectivity in the neuropathology and pathophysiology of schizophrenia.
    Schizophrenia Research 07/2014; 158(1-3). DOI:10.1016/j.schres.2014.06.011 · 3.92 Impact Factor
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    • "However, this interpretation has been made even when the delayed-match-to-sample task does not include intervening distractors (Schneider et al. 2009; Verrico et al. 2011), which are critical for distinguishing selective memorization from the neighborhood strategy. Even tasks that included intervening distractors often did not repeat those images as the test image (Miller et al. 1993; Woloszyn and Sheinberg 2009). When we trained one monkey to perform a version of Match First where intervening distractors were included in each trial but not repeated as the test image, the monkey seemed to be reporting (with 95% accuracy ) whether or not the test image had been presented recently (cf. "
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    ABSTRACT: Seven monkeys performed variants of two short-term memory tasks that others have used to differentiate between selective and nonselective memory mechanisms. The first task was to view a list of sequentially presented images and identify whether a test matched any image from the list, but not a distractor from a preceding list. Performance was best when the test matched the most recently presented image. Response rates depended linearly on recency of repetition whether the test matched a sample from the current list or a distractor from a preceding list, suggesting nonselective memorization of all images viewed instead of just the sample images. The second task was to remember just the first image in a list selectively and ignore subsequent distractors. False alarms occurred frequently when the test matched a distractor presented near the beginning of the sequence. In a pilot experiment, response rates depended linearly on recency of repetition irrespective of whether the test matched the first image or a distractor, again suggesting nonselective memorization of all images instead of just the first image. Modification of the second task improved recognition of the first image, but did not abolish use of recency. Monkeys appear to perform nonspatial visual short-term memory tasks often (or exclusively) using a single, nonselective, memory mechanism that conveys the recency of stimulus repetition.
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    • "In this study, the temporal resolution of fMRI precludes us from distinguishing between encoding-evoked activity that is sustained throughout maintenance and phasic encoding activity that is reconstituted during maintenance. Evidence exists for both possibilities: work utilizing single unit recording has identified cells that fire persistently throughout the delay (Fuster and Alexander 1971), whereas recent multivariate analyses have revealed that information conveyed by EC neurons may degrade early in the delay and be reconstituted toward the end of the delay (Woloszyn and Sheinberg 2009) "
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    ABSTRACT: The ability to actively maintain information in working memory (WM) is vital for goal-directed behavior, but the mechanisms underlying this process remain elusive. We hypothesized that successful WM relies upon a correspondence between the neural processes associated with stimulus encoding and the neural processes associated with maintenance. Using functional magnetic resonance imaging, we identified regional activity and inter-regional connectivity during stimulus encoding and the maintenance of those stimuli when they were no longer present. We compared correspondence in these neural processes across encoding and maintenance epochs with WM performance. Critically, greater correspondence between encoding and maintenance in 1) regional activity in the lateral prefrontal cortex (PFC) and 2) connectivity between lateral PFC and extrastriate cortex was associated with increased performance. These findings suggest that the conservation of neural processes across encoding and maintenance supports the integrity of representations in WM.
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