Abstract

Introduction

An important property of the human mind is that novel information and repeated information are treated differently. In particular, repeated stimuli tend to receive progressively less processing, and this habituation manifests itself in many ways¹. While the discovery of novelty-seeking behavior extends far back into the history of psychological science, our goal in this paper is to explore the relationship between two particular manifestations that have been exploited in rather different subfields of cognitive science: studies of infant perception and cognition based on novelty preferences in looking time, and studies of adult perception and cognition based on repetition attenuation as measured with functional neuroimaging. The first two sections of this paper selectively review these two varieties of habituation, and the third section notes a nuanced set of similarities between them. The final section then explores ways in which the study of habituation in functional neuroimaging could yield novel insights into the nature of habituation in infant cognition – and vice versa.

Habituation in Infant Cognition

Infants tend to look longer at novel stimuli than at repeated stimuli (for a recent review, see Aslin, 2007)². Initial studies in infant cognition were primarily interested in habituation per se as a measure of simple learning in the youngest infants (e.g. Kagan and Lewis, 1965). In such studies, a single stimulus was repeated several times across trials, and the change in time spent fixating on the stimulus over repetitions served as the measure of habituation. Later studies began employing habituation as a research tool to investigate infants' abilities to discriminate and remember stimuli (e.g. Fagan, 1970; Wetherford and Cohen, 1973; see also Bornstein, 1985; Cohen, 1976; Olson, 1976). Critically, this approach involves examining patterns of fixation for repeated vs. novel stimuli, rather than just the decrease in responsiveness to repeated stimuli alone. The visual paired comparison procedure was an early example of this approach: when presented with two complex visual patterns, infants looked longer at a new pattern compared to one that they had previously seen several times (Fantz, 1964). However, in this case it is unclear whether the increased looking reflects a preference for the novel stimulus or avoidance of the repeated stimulus. This result was nevertheless groundbreaking, as it indicated that infants could discriminate the two alternatives, and had memory for the repeated stimulus.

More standard habituation tasks have convincingly demonstrated novelty preferences by relying on a separate test phase. In such designs, infants are repeatedly familiarized to a single stimulus for a fixed amount of time (e.g. Fagan, 1972), or – because of differences in the rate of habituation across subjects – until their looking time is reduced to a criterion level (typically, when the mean looking time over the last three trials is less than 50% of the mean looking time of the first three trials; see Cohen and Gelber, 1975). After reaching this criterion, infants begin a test phase. Perhaps the simplest test involves comparing the looking time to the habituation stimulus (now repeated again during test) vs. the looking time to a novel stimulus that differs from the habituation stimulus along some dimension, such as stimulus orientation or face identity. If the infant represents this dimension, perceives the difference, and finds the difference to be salient, they will exhibit a novelty preference by looking longer at the novel stimulus (sometimes called dishabituation). The novelty preference is quantified as the amount of extra time that the infant fixated the novel stimulus compared to the familiar stimulus, across trials. Since any systematic preference of this sort would only be possible if the infant can discriminate the two stimuli, this technique has been used extensively to describe the perceptual abilities of infants – for example revealing their ability to discriminate orientation (e.g. Atkinson et al., 1988) or faces (e.g. Young-Browne et al., 1977).

Novelty preferences have also been used to study other types of more complex perceptual and conceptual abilities. In many of these studies, the test phase consists of two stimuli that each differ from the familiarized stimulus along some of the same perceptual dimensions, but differ from each other along a critical additional dimension. Again, if infants discriminate this critical dimension, then they may look longer at the stimulus that is novel in this key respect. For example, this technique has been used to explore infants' understanding of simple physical principles – that objects exist even when unseen (the idea of “object permanence”), and cannot pass through each other (e.g. Baillargeon, 1987; Baillargeon et al., 1985; Spelke et al., 1992).

In one such study (Baillargeon, 1987), young infants were familiarized to a display in which a screen lying flat and facing the infant rotated up and away from the infant 180° in the manner of a drawbridge (Figure ​(Figure1A).1A). This motion repeated until a habituation criterion was reached. At test, a new object was then placed at the far edge of the screen, which either did or did not interact with the rotating screen. In “impossible” test displays, the screen moved exactly as during familiarization, appearing to rotate right through the object. In “possible” test displays, the screen rotated only to the point where adults would expect it to contact the object and stop moving. Thus, both test displays were novel (containing a new object), but the “possible” event was more perceptually novel (containing a different screen rotation). Thus, if infants exhibit a perceptual novelty preference, they should look longer at the possible event. However, if they can discriminate the more abstract change (i.e. that the screen violated the principle of object permanence), and if they find this abstract change to be especially salient, then their looking times should increase to the impossible event. Indeed, infants looked longer at the “impossible” test trials (Figure ​(Figure1B)1B) – which was interpreted in terms of a violation of infants' expectations regarding solidity and/or object permanence.

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Figure 1

An example of habituation in infant cognition (adapted from Baillargeon, 1987). (A) Side view of habituation and test displays. In both conditions, infants were habituated to a 180° drawbridge-like motion. The decline and plateau of looking times during habituation are depicted in the left panels of (B). In the Experimental Condition, infants completed two types of test trials, both of which contained a new object on the far side of the display (depicted by the black box). The Impossible Test involved the same full 180° rotation from habituation, but now the screen surprisingly passed through the box as it completed its rotation (with the box disappearing as it became obscured). The Possible Test involved a novel shorter rotation of screen up to the point where it would contact the box, where it stopped; this motion was “possible” in terms of solidity and object permanence, but was more perceptually novel than the Impossible Test. In the Control Condition, the screen rotations were identical, but no new object was presented (such that both motions were equally possible). Within each condition, the two types of test trials were alternated, with order counterbalanced across infants. The results from the test phase are depicted in the right panels of (B). In the Experimental Condition, infants dishabituated to the Impossible Test but not the Possible Test. However, in the Control Condition no preference was observed. These results were interpreted as reflecting the violation of infants' expectations regarding solidity and/or object permanence.

Similar violation-of-expectation studies using looking-time measures have explored many cognitive abilities of preverbal infants, in some cases without using a separate familiarization phase (e.g. Baillargeon, 2000; Wang et al., 2004). For example, one such study examined infants' simple arithmetic abilities (Wynn, 1992). In an “addition” condition, infants were presented with a single familiarization event in which a doll appeared on a stage, a screen rotated up and covered part of the stage, then another doll was placed behind the screen. The screen was then removed to reveal either one or two dolls on the stage. Infants looked longer at the single doll display, which was interpreted in terms of the arithmetic expectation that 1+1=2. Similar evidence of arithmetic competence was found with 1+1=2-or-3 and 2−1=1-or-2 conditions. There has been substantial debate about how these studies that employ limited familiarization (e.g. Wynn, 1992) relate to those in which infants are habituated to criterion (e.g. Baillargeon, 1987). In particular, it has been argued that looking times following limited familiarization may reflect perceptual familiarity preferences rather than conceptual novelty preferences (e.g. Bogartz et al., 1997; Cohen and Marks, 2002). Nevertheless, we mention violation-of-expectation studies here because they do often involve a similar design with repeated vs. novel displays.

These studies collectively illustrate the power of habituation and novelty preferences as phenomena that have been exploited to make inferences about infants' perceptual and cognitive abilities.

Habituation in Functional Neuroimaging

Neural responses tend to be stronger to novel information than to repeated information (for recent reviews, see Grill-Spector et al., 2006; Krekelberg et al., 2006; Schacter et al., 2007). This effect was initially observed in terms of reduced firing rates in single unit recordings from macaque inferior temporal cortex (e.g. Baylis and Rolls, 1987; Brown et al., 1987; Li et al., 1993; Miller and Desimone, 1994), but we will largely focus here on analogous effects observed in functional magnetic resonance imaging (fMRI) of human adults – the phenomenon of repetition attenuation. In typical studies of rapid repetition attenuation (often called fMR-adaptation), each trial contains two images presented 300–500ms apart. Following the presentation of the first image – which serves to familiarize the observer to the stimulus – the second image is either identical to the first image (repeated) or different along some dimension under investigation (novel). For example, the two images may have identical or different local contours (Figure ​(Figure2A).2A). Given the poor temporal resolution of fMRI, the aggregated hemodynamic response to both images is then analyzed. Repetition attenuation can then be quantified as the difference in the hemodynamic response between trials containing identical vs. different images.

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Figure 2

An example of habituation in functional neuroimaging (adapted from Kourtzi and Kanwisher, 2001). (A) In each trial, two stimuli were presented sequentially (each for 300ms with a 400ms pause in between). The stimuli were simple shapes presented behind or in front of three partially occluding bars. In the Repeated trials, the same shape was repeated at the same depth with respect to the occluders. In the Novel Contour trials, the same shape was repeated, but moved in depth with respect to the occluders, such that the local visible contours changed. In the Novel Contour+Shape trials, a different shape was presented as the second stimulus, also moved in depth with respect to the occluders. (B) Event-related fMRI responses to the pairs of stimuli in a region of ventral visual cortex that responds more strongly to objects than to other stimulus patterns (lateral occipital complex; LOC). The response to the Novel Contour trials was the same as the response to the Repeated trials, demonstrating that the LOC does not represent visible local contours per se. However, the responses to both of these conditions were attenuated relative to the response to the Novel Contour+Shape condition. These results suggest that the LOC represents perceived shape rather than local contours.

Because fMRI typically provides data from many regions in the brain, we can consider how brain regions differ with respect to the amount of repetition attenuation they exhibit. In the example depicted in Figure ​Figure2A,2A, if a population of neurons in one region does not represent local contours (such that it cannot discriminate two images on the basis of these contours), the fMRI response in this region will be the same for trials containing identical vs. different contours, and thus there will be no repetition attenuation. The same neuronal population may represent some other property of the stimuli (such that, for example, it can discriminate between two images on the basis of perceived shape); in these cases, the fMRI response in this region will be reduced for trials containing identical vs. different shapes, and thus exhibit repetition attenuation. Both of these patterns are apparent in Figure ​Figure2B2B (adapted from Kourtzi and Kanwisher, 2001).

Repetition attenuation is not an all-or-none affair, of course: the amount of attenuation within a particular brain region is proportional to the degree of selectivity along a given dimension and the magnitude of the difference between two stimuli along that dimension. For example, representations of objects in the lateral occipital complex (LOC; Malach et al., 1995) are orientation-specific: rotating an identical object 15° elicits a greater fMRI response (i.e. less repetition attenuation) than if the object had been repeated in its original orientation, but rotating an identical object 45° elicits an even greater response (Murray and Wojciulik, 2004). Similar parametric methods have also been used to study aspects of cognition, for example revealing a representation of approximate number in intraparietal sulcus (Piazza et al., 2004), and revealing a representation of how similar another person is to oneself in ventromedial prefrontal cortex (Jenkins et al., 2008).

Repetition attenuation is a prevalent consequence of stimulus repetition, and can be observed in modalities other than vision (e.g. Bergerbest et al., 2004; Dehaene-Lambertz et al., 2006), and in various brain regions (e.g. Breiter et al., 1996; Jenkins et al., 2008; Thompson-Schill et al., 1999). Moreover, it is not limited to situations in which the repeated stimulus is presented immediately following the initial stimulus. In fact, attenuated hemodynamic responses to repeated stimuli can be observed after one or more interleaved novel stimuli (e.g. Turk-Browne et al., 2006), or after significant interference (e.g. Henson et al., 2004) and delays (van Turennout et al., 2000). In these cases, hemodynamic responses are individually estimated for the repeated stimulus (rather than the pair, as in the rapid repetition case described above) and compared to the hemodynamic responses for novel stimuli that are presented during that same phase of the experiment. However, note that repetition attenuation is not universal, and many factors contribute to whether or not it will be observed, including selective attention (e.g. Yi and Chun, 2005), task context (e.g. Dobbins et al., 2004; cf. Xu et al., 2007) and explicit recognition (e.g. Schott et al., 2005). Thus, repetition attenuation is most readily observed when stimuli are attended, but repetitions can nevertheless be incidental to the task at hand (e.g. during orthogonal categorization judgments; Dobbins et al., 2004; Turk-Browne et al., 2006).

These examples collectively illustrate the power of habituation in adult cognitive neuroscience as a phenomenon that can be exploited to make inferences about the nature of perceptual and cognitive representations.

The Analogy

The two types of habituation described above are superficially similar, each reflecting a type of decreased responsiveness to repeated stimuli. In the case of infant cognition, infants may be repeatedly familiarized to a stimulus until a preset habituation criterion is met. They are then presented with test stimuli that are more or less similar to the familiarized stimulus in various ways. Looking-time preferences for novel stimuli over repeated stimuli serve as the primary dependent measure, and indicate both that the infant can discriminate along the dimension that distinguishes the test items, and that they have memory for the repeated stimulus. In the case of functional neuroimaging, observers are familiarized to an initial stimulus (typically once, but up to three or more times; e.g. Dobbins et al., 2004; Grill-Spector et al., 1999). They are then presented with a second test stimulus that is more or less similar to the initial stimulus. Attenuated hemodynamic responses within a brain region for repeated stimuli serve as the primary dependent measure, and indicate both that the brain region can discriminate the test items, and that it has represented the repeated stimulus. Thus, both novelty preferences and repetition attenuation reflect increased processing of new information³.

Given that these two subfields of cognitive science have been using similar phenomena as tools to explore similar issues, it is unfortunate that they have typically been treated in isolation. To our knowledge, previous explorations of infant habituation have almost never discussed fMRI repetition attenuation, and vice versa. We think, however, that a theoretical comparison of these two literatures is instructive, since the analogies run deep. Below we review three of these analogies that seem particularly useful to consider in the context of relating these two literatures. It is possible that these analogies suggest a common underlying mechanism for these two forms of habituation, but we will argue that comparing these two literatures is of considerable use and interest even if different but analogous mechanisms are involved.

Exploring the Analogy

The primary goal of this paper has been to highlight an analogy between certain phenomena, methods, results, and mechanisms from two very different literatures. This alone seems worthwhile: the points of connection between habituation as it is used in infant cognition and functional neuroimaging are remarkable, despite the fact that these two phenomena have not been previously connected in this way. But the hope is that this analogy could itself facilitate progress in each area, and serve as a novel type of case study of how neuroscience and infant cognition may usefully interact.

Perhaps the most obvious way to pursue this interaction would be to empirically compare and contrast looking time novelty preferences and fMRI repetition attenuation in the same population. At present, exploring fMRI repetition attenuation in young infants poses considerable methodological challenges, including generic problems of head-motion and loud noise in the scanner, as well as the likelihood that such factors would themselves influence looking-time responses. As technology advances and new methodologies are developed, however, it may become feasible to obtain reliable fMRI data from young infants – in which case it would be fascinating to explore neural responses in the infant brain to the same displays that have been used in looking-time studies⁷.

The alternative – obtaining looking-time data from adults – is also methodologically challenging, for equally important but more abstract reasons. The goal of such a comparison would be to study the same underlying processes in both infants and adults. In general, however, it is rarely possible to achieve this goal in different populations by employing identical stimuli; instead, studying the same processes in two populations often requires using very different displays and tools, since the same displays would bring online different types of processes and strategies for the different populations. This possibility is clear in the present context, since adults' looking times – especially to the kinds of simple displays that are characteristic of infant looking-time studies – would surely reflect many different processes beyond those active in infants. For example, when viewing such displays adults' looking times would be influenced by their higher-level questions about how the experimenters managed to create a seemingly-impossible event, what the experiment is testing, etc. As a result, studies of adult looking behavior in simple displays have not typically been able to obtain meaningful results from looking time per se, and have focused instead on where adults will first fixate upon initially encountering a possibly-repeated display (e.g. Manns et al., 2000; Snyder et al., 2008). More generally, the displays used in infant studies may suffice to attract infants' attention repeatedly, but more complex displays may be required to obtain meaningful looking time data from adults (e.g. Ryan et al., 2007). Thus, equating the same underlying processing in these populations might actually require quite different paradigms and displays.

Though comparisons of these two forms of habituation in the same population resist straightforward empirical testing, such comparisons can nevertheless suggest potentially useful future directions. We conclude by noting four such possibilities:

First, beyond the connections noted above, these literatures are each quite rich, and each contains many manipulations and questions that could be usefully imported into the other. In this way, the analogy could be of great heuristic use, by suggesting new questions for each domain. For example, the role of attention in habituation has been treated very differently in the two literatures. In functional neuroimaging, attention is manipulated via task demands and is typically characterized in terms of resources (e.g. Pessoa et al., 2002) and selection (e.g. O'Craven et al., 1999). Although fMRI habituation is relatively implicit and automatic – such that it can occur despite depleted resources (Yi et al., 2004) – selective attention is nevertheless required (Eger et al., 2004; Murray and Wojciulik, 2004; Vuilleumier et al., 2005; Yi and Chun, 2005). In infant cognition, attention is often characterized in terms of passive states of arousal, for example as measured by heart rates (e.g. Richards, 1997) and manipulated by feeding (e.g. Geva et al., 1999). These states of arousal affect the rate of habituation: after equivalent amounts of exposure, infants exhibit novelty preferences during sustained attention and after feeding, but familiarity preferences during casual attention and prior to feeding (Geva et al., 1999; Richards, 1997). It may be worthwhile to import these different notions of attention into each domain. For example, we know of no direct research in functional neuroimaging on the relationship between arousal and habituation. One promising approach may be to examine how low-frequency shifts in the fMRI signal – that are believed to reflect arousal (Chawla et al., 1999) and other cognitive states (Leber et al., 2008) – influence repetition attenuation (Turk-Browne et al., 2006).

Second, the exploration of this analogy could help to elucidate the underlying cognitive processes that are involved in mediating various types of habituation. In functional neuroimaging, for example, habituation has been interpreted with regard to different forms of memory depending on the lag between repetitions: attenuated responses to repetitions after minimal delays or interruption may reflect short-term transient changes in stimulus-specific processing, while attenuated responses to repetitions over significant delays and interruption may result from long-term learning (see Grill-Spector et al., 2006; Henson, 2003). In contrast, habituation in infant cognition has often been interpreted in terms of the exercise of explicit knowledge (e.g. Spelke, 1988) vs. implicit visual processing (e.g. Cheries et al., in press; Feigenson et al., 2002; Scholl and Leslie, 1999), and has been related to constructs from vision science, such as “object files” (e.g. Carey and Xu, 2001; Cheries et al., 2006; Chiang and Wynn, 2000; Feigenson et al., 2002; Scholl and Leslie, 1999). Thus, it could be of use in each area to consider explanations based on constructs from the other. For example, the finding that looking-time habituation can persist across interruptions by a small number but not a larger number of novel moving objects was interpreted in terms of object files (Cheries et al., 2006), but could also be interpreted in terms of working memory processes, which are similarly capacity-limited. Likewise, while neural repetition effects decline as the lag between repetitions increases (Henson et al., 2004), no research has examined whether such effects are sensitive to the complexity of the intervening items per se.

Third, our understanding of habituation itself may be enhanced by considering the analogy, since different kinds of models have been developed for infant and neural habituation. For example, detailed computational models of infant habituation (e.g. Schoner and Thelen, 2006; Sirois and Mareschal, 2002) could perhaps be supplemented by the neurophysiological accounts of habituation and its consequences that have been invoked in functional neuroimaging, including notions of fatigue (as often invoked in infant habituation), but also learning-related representational changes that result in speeded processing and increased selectivity (see Desimone, 1996; Grill-Spector et al., 2006; Wiggs and Martin, 1998). In particular, increased selectivity and hence reduced neuronal responses may bias competition for limited processing resources to novel stimuli, which evoke larger responses (Desimone and Duncan, 1995; cf. Snyder et al., 2008). In turn, the neurophysiological mechanisms underlying repetition attenuation are relatively unknown (e.g. Sawamura et al., 2006), but may depend heavily on competitive interactions between neurons that are initially broadly-tuned (see Grill-Spector et al., 2006); such ideas, often invoked at the level of mental representations, are an important component of models of infant habituation and development (e.g. Johnson, 2000; Westermann et al., 2007). Thus, an integration of models in the two domains could help us understand the dynamics of habituation in each case.

Fourth, it remains possible that that these two forms of habituation, despite their differences, may reflect the same types of underlying processes. In this case, exploring the analogy noted here could lead not only to progress in each area due to the heuristic consideration of ideas and models from the other area, but could perhaps unite these two domains. To accomplish this, both forms of habituation could be used as tools to study the same topics, with the goal of evaluating how similar the results are. For example, stimulus identity in functional neuroimaging (especially of ventral cortex) is typically evaluated in terms of featural and categorical information, whereas identity in infant cognition has often been evaluated with regard to spatiotemporal continuity (regardless of surface features; see Flombaum et al., in press). The analogy noted here, however, suggests that it might thus be useful to investigate both of these ideas with fMRI habituation. And when this was actually done, in fact, the FFA and the LOC were sensitive to both types of “sameness”: in dynamic motion displays, repetition attenuation was observed only when featurally-identical faces were repeated along a spatiotemporally continuous path (Yi et al., 2008). This provides a new way to think about how featural and spatiotemporal information are combined.

It is our hope that attending to this analogy could help us understand the nature and dynamics of habituation in each field, and ultimately help us appreciate the meaning of these similarities across such different areas of cognitive science, as a type of case study of how neuroscience and infant cognition may be mutually informative.

Conflict of Interest Statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Acknowledgments

Footnotes

References