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R Desimone

Publications and source records attributed to R Desimone.

At least 37 records · Page 2Linked to original sources

Responses of neurons in inferior temporal cortex during memory-guided visual search.

Responses of neurons in inferior temporal cortex during memory-guided visual search. J. Neurophysiol. 80: 2918-2940, 1998. A typical scene will contain many different objects, few of which are relevant to behavior at any given moment. Thus attentional mechanisms are needed to select relevant objects for visual processing and control over behavior. We examined this role of attention in the inferior temporal cortex of macaque monkeys, using a visual search paradigm. While the monkey maintained fixation, a cue stimulus was presented at the center of gaze, followed by a blank delay period. After the delay, an array of two to five choice stimuli was presented extrafoveally, and the monkey was rewarded for detecting a target stimulus matching the cue. The behavioral response was a saccadic eye movement to the target in one version of the task and a lever release in another. The array was composed of one "good" stimulus (effective in driving the cell when presented alone) and one or more "poor" stimuli (ineffective in driving the cell when presented alone). Most cells showed higher delay activity after a good stimulus used as the cue than after a poor stimulus. The baseline activity of cells was also higher preceding a good cue, if the animal expected it to occur. This activity may depend on a top-down bias in favor of cells coding the relevant stimulus. When the choice array was presented, most cells showed suppressive interactions between the stimuli as well as strong attention effects. When the choice array was presented in the contralateral visual field, most cells initially responded the same, regardless of which stimulus was the target. However, within 150-200 ms of array onset, responses were determined by the target stimulus. If the target was the good stimulus, the response to the array became equal to the response to the good stimulus presented alone. If the target was a poor stimulus, the response approached the response to that stimulus presented alone. Thus the influence of the nontarget stimulus was eliminated. These effects occurred well in advance of the behavioral response. When the array was positioned with stimuli on opposite sides of the vertical meridian, the contralateral stimulus appeared to dominate the response, and this dominant effect could not be overcome by attention. Overall, the results support a "biased competition" model of attention, according to which 1) objects in the visual field compete for representation in the cortex, and 2) this competition is biased in favor of the behaviorally relevant object by virtue of "top-down" feedback from structures involved in working memory.

Animals↗

Neural mechanisms of spatial selective attention in areas V1, V2, and V4 of macaque visual cortex.

Many neurons in extrastriate visual cortex have large receptive fields, and this may lead to significant computational problems whenever multiple stimuli fall within a single field. Previous studies have suggested that when multiple stimuli fall within a cell's receptive field, they compete for the cell's response in a manner that can be biased in favor of attended stimuli. In the present study we examined this role of attention in areas V1, V2, and V4 of macaque monkeys with the use of a behavioral paradigm in which attention was directed to one of two stimulus locations. When two stimuli were presented simultaneously inside the cell's receptive field (which could be accomplished only in areas V2 and V4), we found that the cell's response was strongly influenced by which of the two stimuli was attended. The size of this attention effect was reduced when the attended and ignored stimuli were presented sequentially rather than simultaneously. In addition, the effects became very weak and inconsistent in these areas when only one of the two stimuli was located inside the receptive field. Attention thus modulated sensory responses primarily when two or more simultaneous stimuli competed for access to a neuron's receptive field. As in areas V2 and V4, attention did not modulate sensory responses in area V1 when only a single stimulus was inside the receptive field. In addition, the small receptive fields in this area precluded the simultaneous presentation of attended and ignored stimuli inside the receptive field, making it impossible to determine whether attention effects would be observed under the conditions that led to consistent attention effects in areas V2 and V4. Spontaneous firing rates in areas V2 and V4 were found to be 30-40% higher when attention was directed inside rather than outside the receptive field, even when no stimulus was present in the receptive field. Spontaneous firing rates also varied according to the particular location within the receptive field that was attended. These shifts in spontaneous activity may reflect a top-down signal that biases responses in favor of stimuli at the attended location.

Animals↗

Object and place memory in the macaque entorhinal cortex.

Lesions of the entorhinal cortex in humans, monkeys, and rats impair memory for a variety of kinds of information, including memory for objects and places. To begin to understand the contribution of entorhinal cells to different forms of memory, responses of entorhinal cells were recorded as monkeys performed either an object or place memory task. The object memory task was a variation of delayed matching to sample. A sample picture was presented at the start of the trial, followed by a variable sequence of zero to four test pictures, ending with a repetition of the sample (i.e., a match). The place memory task was a variation of delayed matching to place. In this task, a cue stimulus was presented at a variable sequence of one to four "places" on a computer screen, ending with a repetition of one of the previously shown places (i.e., a match). For both tasks, the animals were rewarded for releasing a bar to the match. To solve these tasks, the monkey must 1) discriminate the stimuli, 2) maintain a memory of the appropriate stimuli during the course of the trial, and 3) evaluate whether a test stimulus matches previously presented stimuli. The responses of entorhinal cortex neurons were consistent with a role in all three of these processes in both tasks. We found that 47% and 55% of the visually responsive entorhinal cells responded selectively to the different objects or places presented during the object or place task, respectively. Similar to previous findings in prefrontal but not perirhinal cortex on the object task, some entorhinal cells had sample-specific delay activity that was maintained throughout all of the delay intervals in the sequence. For the place task, some cells had location-specific maintained activity in the delay immediately following a specific cue location. In addition, 59% and 22% of the visually responsive cells recorded during the object and place task, respectively, responded differently to the test stimuli according to whether they were matching or non-matching to the stimuli held in memory. Responses of some cells were enhanced to matching stimuli, whereas others were suppressed. This suppression or enhancement typically occurred well before the animals' behavioral response, suggesting that this information could be used to perform the task. These results indicate that entorhinal cells receive sensory information about both objects and spatial locations and that their activity carries information about objects and locations held in short-term memory.

Analysis of Variance↗

Neural mechanisms for visual memory and their role in attention.

Recent studies show that neuronal mechanisms for learning and memory both dynamically modulate and permanently alter the representations of visual stimuli in the adult monkey cortex. Three commonly observed neuronal effects in memory-demanding tasks are repetition suppression, enhancement, and delay activity. In repetition suppression, repeated experience with the same visual stimulus leads to both short- and long-term suppression of neuronal responses in subpopulations of visual neurons. Enhancement works in an opposite fashion, in that neuronal responses are enhanced for objects with learned behavioral relevance. Delay activity is found in tasks in which animals are required to actively hold specific information "on-line" for short periods. Repetition suppression appears to be an intrinsic property of visual cortical areas such as inferior temporal cortex and is thought to be important for perceptual learning and priming. By contrast, enhancement and delay activity may depend on feedback to temporal cortex from prefrontal cortex and are thought to be important for working memory. All of these mnemonic effects on neuronal responses bias the competitive interactions that take place between stimulus representations in the cortex when there is more than one stimulus in the visual field. As a result, memory will often determine the winner of these competitions and, thus, will determine which stimulus is attended.

Animals↗

Neural mechanisms of visual working memory in prefrontal cortex of the macaque.

Prefrontal (PF) cells were studied in monkeys performing a delayed matching to sample task, which requires working memory. The stimuli were complex visual patterns and to solve the task, the monkeys had to discriminate among the stimuli, maintain a memory of the sample stimulus during the delay periods, and evaluate whether a test stimulus matched the sample presented earlier in the trial. PF cells have properties consistent with a role in all three of these operations. Approximately 25% of the cells responded selectively to different visual stimuli. Half of the cells showed heightened activity during the delay after the sample and, for many of these cells, the magnitude of delay activity was selective for different samples. Finally, more than half of the cells responded differently to the test stimuli depending on whether they matched the sample. Because inferior temporal (IT) cortex also is important for working memory, we compared PF cells with IT cells studied in the same task. Compared with IT cortex, PF responses were less often stimulus-selective but conveyed more information about whether a given test stimulus was a match to the sample. Furthermore, sample-selective delay activity in PF cortex was maintained throughout the trial even when other test stimuli intervened during the delay, whereas delay activity in IT cortex was disrupted by intervening stimuli. The results suggest that PF cortex plays a primary role in working memory tasks and may be a source of feedback inputs to IT cortex, biasing activity in favor of behaviorally relevant stimuli.

Animals↗

Responses of cells in the superior colliculus during performance of a spatial attention task in the macaque.

Previous studies have reported that superficial layer cells in the superior colliculus (SC) give an enhanced response to a stimulus when it is the target for an eye movement. However, in a peripheral detection paradigm, no such enhancement was found when a stimulus was attended, in the absence of an eye movement. Inasmuch as behavioral studies have found attention deficits in the absence of eye movements following SC lesions or deactivation, we investigated this issue in a paradigm that is very sensitive to effects of attention. In a matching-to-sample paradigm, a sample stimulus was presented at one location followed by a brief test stimulus at that (relevant) location and a distracter at another (irrelevant) location. While maintaining fixation, the monkey indicated whether the sample and the test stimulus matched, ignoring the distracter. The relevant and irrelevant locations were switched from trial to trial. SC cells in the superficial layers tended to give enhanced responses when the attended test stimulus was inside the receptive field compared to when the (physically identical) distracter was inside the field. We found that responses to attended targets in the receptive field were larger than to physically identical, but ignored, distracter stimuli. These effects were found only in an "automatic" attentional cueing paradigm, in which a peripheral stimulus explicitly cued the animal as to the relevant location in the receptive field. No attentional effects were found in a "central" or "cognitive" cueing paradigm, in which the monkey had to learn the relevant location in a given block of trials. The larger responses to attended targets in the automatic cueing paradigm appeared to be due to a sustained elevation of cells' baseline activity when attention was directed to the receptive field, as well as a transient enhancement of the target response. Thus, responses of SC cells appear to be modulated by directed attention, even in absence of eye movements, probably reflecting the properties of cortical cells projecting to the SC.

Animals↗

Responses of cells in monkey visual cortex during perceptual filling-in of an artificial scotoma.

When we view a scene through one eye, we typically do not see the scotomas created by the optic disc and the blood vessels overlying the retinal surface. Similarly, when a texture field containing a hole is steadily viewed in peripheral vision (artificial scotoma), the hole appears to fill in with the surrounding texture in a matter of seconds, demonstrating that the visual system fills in information across regions where no information is available. Here we show that, in monkeys viewing a similar texture field with a hole, the responses of extrastriate visual neurons with receptive fields covering the hole increase gradually to a level comparable to that elicited by the same texture without a hole. The time course of these dynamic changes in activity parallels the time course of perceived filling-in of the hole by human observers, suggesting that this process mediates perceptual filling-in.

Animals↗

Responses of cells in the tail of the caudate nucleus during visual discrimination learning.

1. The tail of the caudate nucleus and adjacent ventral putamen (ventrocaudal neostriatum) are major projection sites of the extrastriate visual cortex. Visual information is then relayed, directly or indirectly, to a variety of structures with motor functions. To test for a role of the ventrocaudal neostriatum in stimulus-response association learning, or habit formation, neuronal responses were recorded while monkeys performed a visual discrimination task. Additional data were collected from cells in cortical area TF, which serve as a comparison and control for the caudate data. 2. Two monkeys were trained to perform an asymmetrically reinforced go-no go visual discrimination. The stimuli were complex colored patterns, randomly assigned to be either positive or negative. The monkey was rewarded with juice for releasing a bar when a positive stimulus was presented, whereas a negative stimulus signaled that no reward was available and that the monkey should withhold its response. Neuronal responses were recorded both while the monkey performed the task with previously learned stimuli and while it learned the task with new stimuli. In some cases, responses were recorded during reversal learning. 3. There was no evidence that cells in the ventrocaudal neostriatum were influenced by the reward contingencies of the task. Cells did not fire preferentially to the onset of either positive or negative stimuli; neither did cells fire in response to the reward itself or in association with the motor response of the monkey. Only visual responses were apparent. 4. The visual properties of cells in these structures resembled those of cells in some of the cortical areas projecting to them. Most cells responded selectively to different visual stimuli. The degree of stimulus selectivity was assessed with discriminant analysis and was found to be quantitatively similar to that of inferior temporal cells tested with similar stimuli. Likewise, like inferior temporal cells, many cells in the ventrocaudal neostriatum had large, bilateral receptive fields. Some cells had "doughnut"-shaped receptive fields, with stronger responses in the periphery of both visual fields than at the fovea, similar to the fields of some cells in the superior temporal polysensory area. Although the absence of task-specific responses argues that ventrocaudal neostriatal cells are not themselves the mediators of visual learning in the task employed, their cortical-like visual properties suggest that they might relay visual information important for visuomotor plasticity in other structures. (ABSTRACT TRUNCATED AT 400 WORDS)

Animals↗

Parallel neuronal mechanisms for short-term memory.

Although objects that have just been seen may persist in memory automatically for a time and interact passively with incoming stimulation, some tasks require that the memory be actively maintained and used. To test for the existence of separate automatic and volitional mechanisms of short-term memory, recordings were made from neurons in the inferior temporal cortex of monkeys while the monkeys held a sample picture "in mind" and signaled when it was repeated in a sequence of pictures, ignoring other stimulus repetitions. Some neurons were suppressed by any picture repetition, regardless of relevance, whereas others were enhanced, but only when a picture matched the sample. Short-term memory appears to reflect the parallel operation of these two mechanisms--one being automatic and the other active.

Analysis of Variance↗

Cortical connections of inferior temporal area TEO in macaque monkeys.

In macaque monkeys, lesions involving the posterior portion of the inferior temporal cortex, cytoarchitectonic area TEO, produce a severe impairment in visual pattern discrimination. Recently, this area has been shown to contain a complete, though coarse, representation of the contralateral visual field (Boussaoud, Desimone, and Ungerleider: J. Comp. Neurol. 306:554-575, '91). Because the inputs and outputs of area TEO have not yet been fully described, we injected a variety of retrograde and anterograde tracers into 11 physiologically identified sites within TEO of seven rhesus monkeys and analyzed the areal and laminar distribution of its cortical connections. Our results show that TEO receives feedforward, topographically organized inputs from prestriate areas V2, V3, and V4. Additional sparser feedforward inputs arise from areas V3A, V4t, and MT. Each of these inputs is reciprocated by a feedback projection from TEO. TEO was also found to have reciprocal intermediate-type connections with the fundus of the superior temporal area (area FST), cortex in the most posteromedial portion of the superior temporal sulcus (the posterior parietal sulcal zone [area PP]), cortex in the intraparietal sulcus (including the lateral intraparietal area [area LIP]), the frontal eye field, and area TF on the parahippocampal gyrus. The connections with V3A, V4t, and PP were found only after injections in the peripheral field representations of TEO. Finally, TEO was found to project in a feedforward pattern to area TE and to areas anterior to FST on the lateral bank and floor of the superior temporal sulcus (areas TEm, TEa, and IPa, Seltzer and Pandya: Brain Res. 149:1-24, '78), all of which send feedback projections to TEO. Feedback projections also arise from parahippocampal area TH, and areas TG, 36, and possibly 35. These are complemented by only sparse feedforward projections to TG from central field representations in TEO and to TH from peripheral field representations. The results thus indicate that TEO forms an important link in the occipitotemporal pathway for object recognition, sending visual information forward from V1 and prestriate relays in V2-V4 to anterior inferior temporal area TE.

Animals↗

A neural basis for visual search in inferior temporal cortex.

We often search for a face in a crowd or for a particular object in a cluttered environment. In this type of visual search, memory interacts with attention: the mediating neural mechanisms should include a stored representation of the object and a means for selecting that object from among others in the scene. Here we test whether neurons in inferior temporal cortex, an area known to be important for high-level visual processing, might provide these components. Monkeys were presented with a complex picture (the cue) to hold in memory during a delay period. The cue initiated activity that persisted through the delay among the neurons that were tuned to its features. The monkeys were then given 2-5 choice pictures and were required to make an eye movement to the one (the target) that matched the cue. About 90-120 milliseconds before the onset of the eye movement to the target, responses to non-targets were suppressed and the neuronal response was dominated by the target. The results suggest that inferior temporal cortex is involved in selecting the objects to which we attend and foveate.

Animals↗

Scopolamine affects short-term memory but not inferior temporal neurons.

Effects of scopolamine on performance of a delayed matching-to-sample task and on the properties of neurons in anterior-ventral inferior temporal (IT) cortex were examined in two monkeys. Both monkeys were impaired on the task after systemic administration of scopolamine, suggesting that scopolamine disrupts recency memory. Despite the behavioral deficit, neurons in IT cortex, a region having an important role in visual memory and neuronal properties consistent with that role, were largely unaffected by scopolamine. This dissociation between the behavioral and neuronal effects of scopolamine indicates that the drug either acts at a different site or disrupts unobserved mechanisms at the IT site.

Algorithms↗

The representation of stimulus familiarity in anterior inferior temporal cortex.

1. The inferior temporal (IT) cortex plays an important role in both short- and long-term memory for visual patterns. Most previous studies of IT neurons have tested their responses in recency memory tasks, which require that the memory lasts only the length of a single behavioral trial, which may be < 1 s. To determine the role of IT neurons in longer lasting memories, we measured their responses to initially novel stimuli as the stimuli gradually became familiar to the animal. 2. Two rhesus monkeys were trained on a delayed matching to sample (DMS) task with several intervening stimuli between the sample and the final matching stimulus on each trial. The purpose of the task was to ensure that the animal attended to the stimuli and held them in memory, at least temporarily. Unlike in several previous studies, the focus was not on within-trial effects but rather on the incidental memories that built up across trials as the stimuli became familiar. Each cell was tested with a set of 20 novel stimuli (digitized pictures of objects) that the monkey had not seen before. These stimuli were used in a fixed order over the course of an hour-long recording session, and the number of intervening trials between repetitions of a given sample stimulus was varied. 3. The responses of about one-third of the cells recorded in anterior-ventral IT cortex declined systematically as the novel stimuli became familiar. After six to eight repetitions, responses reached a plateau that was approximately 40% of the peak response. Virtually all of these cells also showed selectivity for particular visual stimuli and thus were not "novelty detectors" in the sense of cells that respond to any novel stimulus. Rather, the responses of these cells were a joint function of familiarity and specific object features such as shape and color. A few cells showed increasing responses with repetition over the recording session, but these changes were accompanied by changes in baseline firing rate, suggesting that they were caused by nonspecific effects. 4. The decrement in response with familiarity was stimulus specific and bridged > 150 presentations of other stimuli, the maximum tested. For some cells the maximum decrement in response occurred for those stimuli that initially elicited the largest response. There was no significant change in response to stimuli that were already familiar. 5. The same cells that showed familiarity effects also showed reduced responses to the matching stimuli at the end of each trial, compared with the responses to the samples.(ABSTRACT TRUNCATED AT 400 WORDS)

Animals↗

The modular organization of projections from areas V1 and V2 to areas V4 and TEO in macaques.

In addition to the major anatomical pathways from V1 into the temporal lobe, there are other smaller, "bypass" routes that are poorly understood. To investigate the direct projection from V1 to V4 (bypassing V2) and from V2 to TEO (bypassing V4), we injected the foveal and parafoveal representations of V4 and TEO with different retrograde tracers in five hemispheres of four macaques and analyzed the distributions of labeled neurons in V1 and V2 using flattened preparations of the cortex. In V1, labeled neurons were seen after injections in V4 but not TEO. The V4-projecting neurons were located in the foveal representation of V1, in both cytochrome oxidase (CO)-rich blobs and CO-poor interblob regions. In V2, TEO-projecting neurons were intermingled with V4-projecting neurons, although the former were far sparser than the latter. Across the cases, 6-19% of the TEO-projecting neurons were double labeled, that is, also projected to area V4. Both V4- and TEO-projecting neurons formed bands that ran orthogonal to the V1/V2 border, and both were located in CO-rich thin stripes and CO-poor interstripe regions. In some cases, a continuous band of V4-projecting neurons was also found along the V1/V2 border in the foveal representation of V2. The results indicate that the pathways from V1 to V4 and from V2 to TEO involve anatomical subcompartments thought to be concerned with both color and form. These "bypass" routes may allow coarse information about color and form to arrive rapidly in the temporal lobe. The bypass route from V2 to TEO might explain the partial sparing of color and form vision that is seen after lesions of V4. By analogy, given the bypass route from the foveal representation of V1 to V4, lesions of V2 affecting the foveal visual field would also be insufficient to block color and form vision.

Amidines↗

Activity of neurons in anterior inferior temporal cortex during a short-term memory task.

Inferior temporal (IT) cortex of primates is known to play an important role in visual memory. Previous studies of IT neurons during performance of working memory tasks have found modulation of responses when a current stimulus matched an item in memory; however, this effect was lost if other stimuli intervened in the retention interval. To examine how IT cortex retains memories while new stimuli are activating the cells, we recorded from IT neurons while monkeys performed a delayed matching-to-sample task, with multiple intervening items between the sample and matching test stimulus. About half of the cells responded differently to a test stimulus if it matched the sample, and this difference was maintained following intervening stimuli. For most of the affected cells, the responses to matching stimuli were suppressed; however, for a few cells the opposite effect was seen. Temporal contiguity alone could not explain the results, as there was no modulation of responses when a stimulus on one trial was repeated on the next trial. Thus, an active reset mechanism appears to restrict the memory comparison to just the stimuli presented within a trial. The suppressive effects appear to be generated within or before IT cortex since the suppression of response to matching stimuli began almost immediately with the onset of the visual response. The memory of the sample stimulus affected not only the responses to matching stimuli but also those to nonmatching stimuli. There was suggestive evidence that the more similar a nonmatching stimulus to the sample, the more the response was suppressed. About a quarter of the cells showed stimulus-selective activity in the delay interval following the sample. However, this activity appeared to be eliminated by intervening stimuli. Thus, it is unlikely that delay-interval activity in IT contributed to the performance of this particular version of delayed matching to sample. To determine how much information about the match-nonmatch status of the stimulus was conveyed by individual neurons, we analyzed the responses with discriminant analysis. The responses of an individual IT neuron could be used to classify a stimulus as matching or nonmatching on about 60% of the trials. To achieve the same performance as the animal would require averaging the responses of a minimum of 25 IT neurons. There was no evidence that mnemonic information was carried by temporal variations in the spike trains. By contrast, there was a modest amount of temporal variation in sensory responses to different visual stimuli.(ABSTRACT TRUNCATED AT 400 WORDS)

Analysis of Variance↗