Julie Golomb

A Taxonomy of External and Internal Attention

Attention is a core property of all perceptual and cognitive operations. Given limited capacity to process competing options, attentional mechanisms select, modulate, and sustain focus on information most relevant for behavior. A significant problem, however, is that attention is so ubiquitous that it is unwieldy to study. We propose a taxonomy based on the types of information that attention operates over--the targets of attention. At the broadest level, the taxonomy distinguishes between external attention and internal attention. External attention refers to the selection and modulation of sensory information. External attention selects locations in space, points in time, or modality-specific input. Such perceptual attention can also select features defined across any of these dimensions, or object representations that integrate over space, time, and modality. Internal attention refers to the selection, modulation, and maintenance of internally generated information, such as task rules, responses, long-term memory, or working memory. Working memory, in particular, lies closest to the intersection between external and internal attention. The taxonomy provides an organizing framework that recasts classic debates, raises new issues, and frames understanding of neural mechanisms.

The Native Coordinate System of Spatial Attention Is Retinotopic

Visual processing can be facilitated by covert attention at behaviorally relevant locations. If the eyes move while a location in the visual field is facilitated, what happens to the internal representation of the attended location? With each eye movement, the retinotopic (eye-centered) coordinates of the attended location change while the spatiotopic (world-centered) coordinates remain stable. To investigate whether the neural substrates of spatial attention reside in retinotopically and/or spatiotopically organized maps, we used a novel gaze-contingent behavioral paradigm that probed spatial attention at various times after eye movements. When task demands required maintaining a spatiotopic representation after the eye movement, we found facilitation at the retinotopic location of the spatial cue for 100–200 ms after the saccade, although this location had no behavioral significance. This task-irrelevant retinotopic representation dominated immediately after the saccade, whereas at later delays, the task-relevant spatiotopic representation prevailed. However, when task demands required maintaining the cue in retinotopic coordinates, a strong retinotopic benefit persisted long after the saccade, and there was no evidence of spatiotopic facilitation. These data suggest that the cortical and subcortical substrates of spatial attention primarily reside in retinotopically organized maps that must be dynamically updated to compensate for eye movements when behavioral demands require a spatiotopic representation of attention. Our conclusion is that the visual systems native or low-level representation of endogenously maintained spatial attention is retinotopic, and remapping of attention to spatiotopic coordinates occurs slowly and only when behaviorally necessary.

Enhanced Visual Motion Perception in Major Depressive Disorder

Major depressive disorder (MDD) is a mood disorder that is not traditionally considered to affect the visual system. However, recent findings have reported decreased cortical levels of the inhibitory neurotransmitter GABA in occipital cortex. To explore possible functional consequences of MDD on visual processing, we applied a psychophysical visual motion processing task in which healthy young adults typically exhibit impaired perceptual discrimination of large high-contrast stimuli. It has been suggested that this phenomenon, spatial suppression, is mediated by GABAergic center–surround antagonism in visual pathways. Based on previous findings linking MDD to occipital GABA dysfunction, we hypothesized that MDD patients would exhibit decreased spatial suppression, leading to the counterintuitive hypothesis of better psychophysical performance. Indeed, motion perception for typically suppressed stimuli was enhanced in patients with MDD compared with age-matched controls. Furthermore, the degree of spatial suppression correlated with an individuals illness load; patients with greater lifetime duration of depression exhibited the least spatial suppression and performed the best in the high-contrast motion discrimination task. Notably, this decrease in spatial suppression persisted beyond recovery and without the confound of acute illness or treatment; all patients had been clinically recovered and unmedicated for several months at the time of testing, suggesting that depression has ubiquitous consequences that may persist long after mood symptoms have receded. This finding raises the possibility that spatial suppression may represent a sensitive endophenotypic marker of trait vulnerability in MDD.

Attentional facilitation throughout human visual cortex lingers in retinotopic coordinates after eye movements.

With each eye movement, the image of the world received by the visual system changes dramatically. To maintain stable spatiotopic (world-centered) visual representations, the retinotopic (eye-centered) coordinates of visual stimuli are continually remapped, even before the eye movement is completed. Recent psychophysical work has suggested that updating of attended locations occurs as well, although on a slower timescale, such that sustained attention lingers in retinotopic coordinates for several hundred milliseconds after each saccade. To explore where and when this “retinotopic attentional trace” resides in the cortical visual processing hierarchy, we conducted complementary functional magnetic resonance imaging and event-related potential (ERP) experiments using a novel gaze-contingent task. Human subjects executed visually guided saccades while covertly monitoring a fixed spatiotopic target location. Although subjects responded only to stimuli appearing at the attended spatiotopic location, blood oxygen level-dependent responses to stimuli appearing after the eye movement at the previously, but no longer, attended retinotopic location were enhanced in visual cortical area V4 and throughout visual cortex. This retinotopic attentional trace was also detectable with higher temporal resolution in the anterior N1 component of the ERP data, a well established signature of attentional modulation. Together, these results demonstrate that, when top-down spatiotopic signals act to redirect visuospatial attention to new retinotopic locations after eye movements, facilitation transiently persists in the cortical regions representing the previously relevant retinotopic location.

Effects of adult aging on utilization of temporal and semantic associations during free and serial recall

Older adults show poorer performance than young adults at word list recall, especially for order information. In contrast with this temporal association deficit, older adults are generally adept at using preexisting semantic associations, when present, to aid recall. We compared the use of temporal and semantic associations in young and older adults’ word list recall following both free recall and serial recall instructions. Decomposition of serial position curves confirmed that older adults showed weakened use of temporal context in recall in relation to young adults, a difference that was amplified in serial recall. Older adults’ temporal associations were also less effective than young adults’ when correlated with serial recall performance. The differential age decrement for serial versus free recall was accompanied by a persistent influence of latent semantic associations in the older adults, even when maladaptive for serial recall.

Attention doesn’t slide: spatiotopic updating after eye movements instantiates a new, discrete attentional locus

During natural vision, eye movements can drastically alter the retinotopic (eye-centered) coordinates of locations and objects, yet the spatiotopic (world-centered) percept remains stable. Maintaining visuospatial attention in spatiotopic coordinates requires updating of attentional representations following each eye movement. However, this updating is not instantaneous; attentional facilitation temporarily lingers at the previous retinotopic location after a saccade, a phenomenon known as the retinotopic attentional trace. At various times after a saccade, we probed attention at an intermediate location between the retinotopic and spatiotopic locations to determine whether a single locus of attentional facilitation slides progressively from the previous retinotopic location to the appropriate spatiotopic location, or whether retinotopic facilitation decays while a new, independent spatiotopic locus concurrently becomes active. Facilitation at the intermediate location was not significant at any time, suggesting that top-down attention can result in enhancement of discrete retinotopic and spatiotopic locations without passing through intermediate locations.

Retinotopic memory is more precise than spatiotopic memory

Successful visually guided behavior requires information about spatiotopic (i.e., world-centered) locations, but how accurately is this information actually derived from initial retinotopic (i.e., eye-centered) visual input? We conducted a spatial working memory task in which subjects remembered a cued location in spatiotopic or retinotopic coordinates while making guided eye movements during the memory delay. Surprisingly, after a saccade, subjects were significantly more accurate and precise at reporting retinotopic locations than spatiotopic locations. This difference grew with each eye movement, such that spatiotopic memory continued to deteriorate, whereas retinotopic memory did not accumulate error. The loss in spatiotopic fidelity is therefore not a generic consequence of eye movements, but a direct result of converting visual information from native retinotopic coordinates. Thus, despite our conscious experience of an effortlessly stable spatiotopic world and our lifetime of practice with spatiotopic tasks, memory is actually more reliable in raw retinotopic coordinates than in ecologically relevant spatiotopic coordinates.

Preservation of episodic visual recognition memory in aging

Abstract Visual episodic recognition memory was assessed in young (mean age 22.5 years) and older (mean age 74.1 years) adults. To isolate purely visual memory, recognition was tested with sets of briefly-presented compound sinusoidal gratings, which minimized age-related differences in visual processing, and resisted verbal encoding. Recognition was measured after delays of 1, 2 or 4 seconds. Overall, neither accuracy of recognition nor speed of response differed significantly between groups, or with probe delay, which strengthens recent claims that visual memory tends to be spared during the course of normal aging.

Complementary attentional components of successful memory encoding

Attention during encoding improves later memory, but how this happens is poorly understood. To investigate the role of attention in memory formation, we combined a variant of a spatial attention cuing task with a subsequent memory fMRI design. Scene stimuli were presented in the periphery to either the left or right of fixation, preceded by a central face cue whose gaze oriented attention to the probable location of the scene. We contrasted activity for scenes appearing in cued versus uncued locations to identify: (1) regions where cuing facilitated processing, and (2) regions involved in reorienting. We then tested how activity in these facilitation and reorienting regions of interest predicted subsequent long-term memory for individual scenes. In facilitation regions such as parahippocampal cortex, greater activity during encoding predicted memory success. In reorienting regions such as right temporoparietal junction, greater activity during encoding predicted memory failure. We interpret these results as evidence that memory formation benefits from attentional facilitation of perceptual processing combined with suppression of the ventral attention network to prevent reorienting to distractors.

Spatial priming in ecologically relevant reference frames

In recent years, researchers have observed many phenomena demonstrating how the visual system exploits spatial regularities in the environment in order to benefit behavior. In this paper, we question whether spatial priming can be considered one such phenomenon. Spatial priming is defined as a response time facilitation to a visual search target when its spatial position has been repeated in recent trials (Maljkovic & Nakayama, 1996, Perception & Psychophysics, 58, 977–991). Does this priming serve a behaviorally adaptive role or is it merely a byproduct of ongoing visual processing? Critically, an adaptive priming mechanism must actively transform visual inputs from native retinotopic (eye-centered) coordinates into ecologically relevant coordinates, e.g., spatiotopic (world-centered) and/or object-centered. In Experiment 1, we tested this hypothesis by having participants move their eyes between trials, which dissociated retinotopic and spatiotopic frames of reference. Results showed only weak retinotopic priming, but robust spatiotopic priming. The second experiment again had participants move their eyes between trials but also manipulated the placement of a grouped array of display objects from trial to trial. This allowed us to measure not just retinotopic and spatiotopic priming, but object-centered priming as well. Results from this experiment did not yield retinotopic priming but showed robust spatiotopic and object-centered priming. These findings demonstrate that spatial priming operates within ecologically relevant coordinate systems, and the findings support the notion that spatial priming serves an adaptive role in human behavior.