What are you looking at?: Impaired ‘social attention’ following frontal-lobe damage

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Abstract

Humans are able to predict the behavior of others. Several studies have investigated this capability by determining if social cues, such as eye gaze direction, can influence the allocation of visual attention. When a viewer sees a face looking to the left, the viewer’s attention is allocated in the gazed-at direction. These ‘social attention’ studies have asked if this allocation of attention is automatic or under voluntary control. In this paper, we show that a patient with frontal-lobe damage is impaired at allocating attention to peripheral locations voluntarily, although attention can be allocated there automatically. The patient, EVR, can use peripheral cues to selectively process one location over another but cannot use symbolic cues (words) to allocate attention. EVR is also impaired in using eye gaze cues to allocate attention, suggesting that ‘social attention’ may involve frontal-lobe processes that control voluntary, not automatic, shifts of visuospatial attention.

Introduction

Humans appear to be endowed with the ability to make predictions regarding others’ behavior or intentions. For example, a professor may predict that an approaching student is going to ask for an extension on an assignment if the assignment is due in 2 days. Some theories label this ability as a “mind reading” ability or a “theory-of-mind” (e.g., Baron-Cohen, 1995, Leslie, 1991; Premack & Woodruff, 1978), and some theories suggest that such an ability allows humans to understand the social interactions that are important in the elaborate social hierarchies of primates (e.g., Cheney & Seyfarth, 1990).

Perception of another person’s eye gaze direction plays a key role in many theory-of-mind theories (e.g., Baron-Cohen, 1995) for several reasons. First, gaze direction may signal the upcoming target or goal of another person’s behavior, which helps predict behavior; for example, chimpanzees appear to be able to use another’s line of gaze to orient attention (Povinelli & Eddy, 1996; Povinelli, Nelson, & Boysen, 1990), although such abilities may not require an attribution of mental states (see Gagliardi, Kirkpatrick-Steger, Thomas, Allen, & Blumberg, 1995; Reaux, Theall, & Povinelli, 1999). Second, gaze perception appears to be supported by gaze-selective neural responses in a “face-cell” area in the superior temporal sulcus of the macaque (Perrett, Hietanen, Oram, & Benson, 1992), an area which may correspond to the “fusiform face area” of human extrastriate cortex (Kanwisher, McDermott, & Chun, 1997). Third, sensitivity to gaze direction emerges in early life (see Vecera & Johnson, 1995 for relevant results), suggesting a role in developing human social skills. Given these reasons, theorists such as Baron-Cohen (1995) hypothesize distinct cognitive modules for detecting eyes and perceiving another’s eye gaze direction. Initial research supporting these theories and processes came from special populations (e.g., children with autism). More recent studies of cognitively normal individuals support theory-of-mind theories by showing that visuospatial attention is influenced by another’s gaze direction (Driver et al., 1999; Friesen & Kingstone, 1998; Kingstone, Friesen, & Gazzaniga, 2000; Langton and Bruce, 1999, Langton and Bruce, 2000).

Previous research on visuospatial attention has demonstrated that attention can be allocated to locations by different types of cues that appear before a target stimulus appears (Posner, 1980; Posner, Snyder, & Davidson, 1980). In Posner’s now-classic task, participants are asked to detect a visual target which appears at a peripheral location. Prior to target onset, a predictive cue appears. “Valid” cues correctly predict a target’s subsequent location, whereas “invalid” cues are inaccurate and misleading. Participants are generally faster to detect validly cued targets than invalidly cued targets. Also, two cue types have been studied in this task, and these cues differ in their effects on attentional orienting. Peripheral cues flicker briefly at the predicted target location, whereas centrally-presented (symbolic) cues indicate a target’s probable location by means of symbolic information such as a word or arrow. Peripheral cues appear to capture spatial attention automatically or reflexively (Jonides, 1981; Yantis & Hillstrom, 1994), cannot be ignored, and are not interfered with by symbolic cues (Jonides, 1981; Müller & Rabbit, 1989). Peripheral cues summon attention even when they do not reliably predict target location; infrequently-occurring validly cued targets are detected faster than frequently-occurring invalidly cued targets. In contrast, symbolic cues require participants to shift attention voluntarily to the cued location. These symbolic cues can be ignored and are interfered with by peripheral cues (Jonides, 1981; Müller & Rabbit, 1989), although these cues need not predict an upcoming target’s location to direct attention to a cued location (Hommel, Pratt, Colzato, & Godijn, 2001; Tipples, 2002).

An important question is whether gaze cues orient spatial attention reflexively, as peripheral cues, or voluntarily, as symbolic cues. If eye gaze is critical to inferring another’s mental state, as suggested by theory-of-mind accounts, then one might expect gaze cues to summon attention automatically to gazed-at locations. This prediction finds some support: When another person’s eyes are gazing to our left, validly cued targets that appear there are processed faster and more accurately than invalidly cued targets that appear to our right (Driver et al., 1999; Friesen & Kingstone, 1998; Langton & Bruce, 1999). Further, eye gaze can affect attentional orienting when a target appears at the gazed-at (validly cued) location infrequently, suggesting that gaze cues orient attention in a reflexive manner. Attention is summoned to a cued (i.e., gazed at) location even when the target is more likely to appear at the uncued (i.e., not gazed at) location. When the gaze cue is counter-predictive, gaze cues, like peripheral cues, cannot be ignored, and attention is driven to the gazed-at location (Driver et al., 1999; Friesen & Kingstone, 1998; Langton & Bruce, 1999).

Several issues remain to be addressed before we conclude that gaze direction cues automatically influence the orienting of spatial attention. For example, if participants in a gaze precuing study are good “mind readers,” they might correctly guess the expected outcome of the experiment and adjust their behavior accordingly (i.e., voluntarily orienting attention in the direction of the gaze cue). Also, in many social situations, reflexive orienting by gaze is inappropriate or unwarranted, such as when a speaker casually glances upward during conversation. Such casual glances differ from more meaningful glances that would be important for attentional allocation. Purely reflexive orienting to gaze would not allow different social contexts to influence attentional allocation; in contrast, voluntary orienting could allow social context to modulate attentional orienting based on gaze direction. Current reflexive accounts of gaze-directed attention do not explain how attention can distinguish between appropriate and inappropriate contexts.

Neuropsychological data can provide additional evidence regarding the orienting produced by eye gaze cues. We focus on patients with frontal-lobe lesions, who exhibit a variety of cognitive impairments that can broadly be classified as problems with cognitive control (see Kimberg, D’Esposito, & Farah, 2000; Miller & Cohen, 2001, for recent reviews). Some of these impairments in cognitive control appear as attentional impairments. Patients with frontal-lobe lesions are distracted by irrelevant stimuli (Chao & Knight, 1995), are impaired at voluntarily sustaining attention (Wilkins, Shallice, & McCarthy, 1987), and are impaired at using advance information in a variety of tasks, including spatial cuing tasks (Alivisatos, 1992; Alivisatos & Milner, 1989; Koski, Paus, & Petrides, 1998). Because frontal-lobe patients do not appear to be impaired in highly-practiced, automatic tasks, these patients can be studied to explore dissociations between automatic and voluntary attentional processes.

Studies investigating voluntary attention in frontal patients have used variants of Posner’s spatial cuing task with symbolic cues. For example, Alivisatos and Milner (1989) presented patients with word cues that either signaled the upcoming target’s location (valid trials) or provided no information about the target’s location (neutral trials). Frontal-lobe patients showed a smaller attentional benefit (the difference in performance between valid and neutral trials) than either control participants or temporal lobe patients. Koski et al. (1998) reported similar results from centrally-presented arrow cues that either validly predicted the upcoming target’s location or did not predict the target’s location. Again, frontal patients showed smaller attentional benefits than both control participants and temporal lobe patients. In the foregoing studies, the frontal patients had varied lesion locations that included dorsolateral and ventromedial frontal areas.

To determine if eye gaze cues orient attention in an automatic or voluntary manner, we investigated attentional orienting in patient EVR, who had regions of both frontal lobes excised during removal of a tumor (Eslinger & Damasio, 1985). EVR performed a simple spatial cuing task in which he detected the onset of a target that appeared in the visual periphery (see Fig. 1). The target was preceded by a spatial cue that either predicted the target’s location (valid cue) or did not predict the target’s location (invalid cue). As shown in Fig. 1, we tested EVR with three types of spatial cues to assess his attentional orienting: peripheral cues, symbolic cues (e.g., words, such as “left”), and gaze cues. Previous findings from frontal-lobe patients (Alivisatos & Milner, 1989; Koski et al., 1998) lead us to hypothesize that EVR would be unable to use symbolic word cues to orient attention. Further, we expected to find that EVR would have no difficulty orienting to peripheral cues because peripheral cues orient attention automatically (e.g., Jonides, 1981; Müller & Rabbit, 1989; Yantis & Jonides, 1984) and because frontal-lobe patients typically do not have impairments in ‘automatic’ performance. The critical issue concerns gaze cues. If gaze cues summon attention automatically, then EVR should be unimpaired orienting to gaze cues. Specifically, he should be faster to detect targets validly cued by gaze than targets invalidly cued by gaze. If gaze cues orient attention in a voluntary manner, however, then EVR should be impaired orienting to gaze cues (in addition to being impaired orienting to symbolic cues).

Section snippets

Case report

At age 35, EVR was diagnosed with a cerebral tumor, a large orbitofrontal meningioma. The tumor was surgically removed, and EVR recovered. EVR’s frontal-lobe damage in the chronic phase of recovery corresponded to regions F07, F11, and F12 in Damasio and Damasio’s (1989) lesion analysis schema. The removal of the tumor and frontal-lobe tissue left EVR with lasting impairments in decision making, personality, and some forms of cognitive control. For example, EVR seems to have an impairment with

Participants

Both EVR and ten older control participants performed a spatial cuing task (Fig. 1) in which a target appeared at a peripheral visual location. Prior to the target, a cue appeared. Three cues were tested in different blocks of trials: peripheral cues, symbolic word cues, and eye gaze cues. The control participants had a mean age of 69.3 years (S.D.=4.6 years).

Stimuli

Participants sat approximately 60 cm from a Macintosh iMac computer (15 in. monitor). Each trial began with a central fixation point and

Control participants

Reaction times (RTs) over 1000 ms were excluded from the analyses as outliers, and this trimming excluded less than 2% of the data. There was no evidence of any systematic anticipatory responses (RTs<150 ms). The control participants made few catch trial errors (<2%). For each participant, we computed the cuing effect across each cue type (peripheral, word, or gaze), collapsed across SOA. The cuing effect was defined as the invalid cue RT minus the valid cue RT; positive scores indicated a cuing

Discussion

EVR demonstrated significant cuing effects to peripheral cues at short cue-target intervals, indicating that his spatial attention can be summoned ‘automatically’ to a peripheral location. However, EVR could not reliably use centrally-presented word cues to allocate visual attention to peripheral locations, despite preserved perception of these cues, replicating the results of previous studies that reported frontal-lobe patients’ inability to orient attention from symbolic cues (Alivisatos &

Acknowledgements

The research in this paper was supported in part by grants from the National Science Foundation (BCS 99-10727), the National Institute of Mental Health (MH60636), the National Institute of Neurological Disease and Stroke (P01 NS19632), and the National Institute of Aging (AG/NS15071). The authors wish to thank Daniel Tranel for sharing data on patient EVR and Steve Luck, Maureen Marron, Morris Moscovitch, and two anonymous referees for useful comments and discussion.

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