By parametrically manipulating the degree of bottom-up perceptual grouping present within multielement displays, a monotonic relationship between the degree of competition and perceptual grouping was found in extrastriate visual cortex, such that grouped stimuli induced less competition. Importantly, these findings build on a previous study, which found that stimuli grouped via illusory contour formation (as used here) or collinear alignment (with oriented gabors) competed less than the same stimuli randomly oriented (McMains and Kastner, 2010
), suggesting that perceptual grouping processes in general counteract competition throughout the visual field. When subjects attended to the peripheral stimulus displays, there was an inverse relationship between attentional modulation and the degree of perceptual grouping present in the multielement display, such that attentional modulation was greatest when neural competition was little influenced by bottom-up mechanisms and smallest when competition was strongly influenced by bottom-up mechanisms. These results are consistent with an account that assumes top-down processes to operate on local neural networks that mediate grouping and competition, thereby providing interfaces to constrain and guide attentional selection (interface hypothesis). Our findings suggest that selective attention counteracts competitive interactions among multiple stimuli that have not been resolved by bottom-up grouping processes.
As noted previously (Kastner et al., 1998
; Beck and Kastner, 2005
), there were several differences between the SEQ and SIM presentation conditions, in addition to the level of competition they induced. For instance, the visual presentation period of the SEQ condition extended over 1 s, whereas the presentation period for the SIM condition was 250 ms. In addition, the SEQ condition contained four visual onsets, whereas the SIM condition contained only one. However, if the stimulus duration, number of onsets, or any other inherent low-level differences between the SEQ and SIM conditions were solely driving the observed difference in activation for the two conditions, then the difference between conditions should be constant across different stimulus configurations. Previously, Kastner et al. (2001)
have found that, within a visual area, the difference between the SEQ and SIM conditions decreased with increasing spatial separation. Similarly, the difference between SEQ and SIM conditions decreased as the perceptual grouping among elements within unattended SIM arrays increased in the current and in a previous (McMains and Kastner, 2010
) experiment, whereas the number of onsets and the stimulus duration were held constant. Importantly, the differences in competition as measured by the SSI observed here were attributable to changes in activity evoked by the SIM conditions in which such factors do not vary.
Previous studies have shown that top-down attentional modulation is greater when stimuli are present simultaneously in the visual field, thereby competing for neural representation, as opposed to when the same stimuli are presented in isolation (Kastner et al., 1998
; Reynolds et al., 1999
). These findings support the biased competition theory, which proposes that top-down processes such as selective attention operate by counteracting competitive interactions among stimuli (Desimone and Duncan, 1995
; Beck and Kastner, 2009
). Here, using a parametric modulation of competition, we extend previous findings by demonstrating that it is not simply the presence or absence of competition that influences the amount of attentional effects, but rather that the degree of attentional modulation is closely tied to the degree of competition left unresolved after automatic bottom-up perceptual grouping processes have occurred and influenced competitive processes. In fact, when the stimulus array was attended to, we found that competitive interactions were similar for all levels of perceptual grouping, suggesting that bottom-up and top-down processes interact dynamically to resolve neural competition to the greatest possible extent.
These results are consistent with several recent physiology studies suggesting that top-down and bottom-up processes interact dynamically in visual cortex (Mazer and Gallant, 2003
; Reynolds and Desimone, 2003
; Bichot et al., 2005
; Ogawa and Komatsu, 2006
). For instance, a study investigating the interaction of bottom-up stimulus contrast and top-down attention in modulating competitive interactions in monkey V4 (Reynolds and Desimone, 2003
), which found a similar inverse relationship between attentional modulation and bottom-up processes. When attention was directed away from a V4 RF, increasing the stimulus contrast of a preferred stimulus within the RF counteracted competition from a neighboring nonpreferred stimulus in the RF. When attention was directed toward the RF, the greatest modulation was observed when competition was little influenced by bottom-up stimulus salience, whereas the least modulation was observed when competition was already counteracted by bottom-up visual salience. In addition, different V4 cells have been found to represent bottom-up visual salience and top-down behavioral relevance (Ogawa and Komatsu, 2006
). Interestingly, in the neural population, the initial visual response was dominated by the bottom-up salience (i.e., the singleton type of the RF stimulus), whereas the late pretarget selection response was dominated by the behavioral significance of the stimulus in the RF, suggesting that top-down and bottom-up signals are dynamically represented within the same population of cells.
Attentional selection within the spatial domain has often been conceptualized with the help of a spotlight metaphor. According to the spotlight hypothesis, top-down processes only operate on neurons that represent the attended locations within the spotlight. The strength of attentional enhancement is thought to be related to the size of the spotlight and difficulty of the task being performed at the attended location (Eriksen and St. James, 1986
). In general, the attentional spotlight does not consider visual information outside the focus of attention such as nearby distracter stimuli that may influence competition or provide contextual information for grouping processes. Alternatively, the interface hypothesis suggests that selective attention operates on interfaces constituted by local networks. The interface hypothesis was first proposed by von der Heydt and colleagues (Qiu et al., 2007
) based on a physiology study that investigated the relationship between bottom-up figure–ground segmentation processes and top-down attention in area V2. They found that, when a monkey directed attention toward the RF of a neuron, attentional modulation was larger when the preferred figure–ground configuration was present within the RF. These findings were interpreted in terms of an interface hypothesis of attention, which proposed that the circuit mediating figure–ground assignment provided an interface within early visual cortex for attentional mechanisms to operate on. According to such an account, the degree of attentional modulation within a region can be predicted by how much the attended stimulus engages local circuits. These results are consistent with the finding that local interneurons that subserve intrinsic circuits receive stronger attentional modulation than other cell classes (Mitchell et al., 2007
Here, we propose that local networks subserving competitive interactions among groups of neurons coding for multiple nearby stimuli may also provide an interface for attentional mechanisms to operate on, although at a different level of processing compared with the studies on figure–ground segmentation (Qiu et al., 2007
). The finding that the amount of attentional modulation was dependent on the output of automatic bottom-up competitive processes may be taken as evidence that the same neural circuits underlie both processes, and that the circuit that mediates competition provides an interface for attentional modulation (Qiu et al., 2007
). Thus, top-down mechanisms might operate on local circuits within V4, an area thought to be important in computing competitive interactions among multiple stimuli (De Weerd et al., 1999
; Gallant et al., 2000
), or on a feedback network that includes V4. Importantly, with fMRI it is often difficult to reveal underlying neural mechanisms. For instance, how might automatic perceptual grouping and competitive processes interact at the neural level? There are two main possibilities, which are not mutually exclusive (McMains and Kastner, 2010
). First, competition in intermediate visual areas, such as V4, may be influenced by perceptual organization processes that occur in early visual cortex (von der Heydt and Peterhans, 1989
; Sheth et al., 1996
; Lee and Nguyen, 2001
; Maertens and Pollmann, 2005
; Montaser-Kouhsari et al., 2007
). These mechanisms could boost the activity related to the set of stimuli as it enters intermediate visual areas such as area V4, which has the larger RF needed to read out biases resulting from perceptual organization computed in early visual cortex and integrate them with parallel competitive processes. A second possibility is that perceptual grouping and competition may rely on the same set of neural mechanisms implemented at intermediate processing stages (Kastner et al., 2001
; Behrmann and Kimchi, 2003
). Regardless of the underlying mechanisms, top-down attention appears to modulate local networks involved in computing competitive processes, given that the largest effects of attention were found when competition among array elements was greatest. Together, the results of Qiu et al. (2007)
and our present results suggest that attention may operate on several different interfaces, which may be recruited at different levels of processing.
The interface hypothesis is similar to a recent proposal by Gilbert and Sigman (2007)
, which suggests that the magnitude of attentional enhancement within a visual area is determined by the degree to which the local circuits computing contextual information are involved in the ongoing computation. Both proposals challenge the traditional view that attention acts in a hierarchical manner, a view based on the finding that attention effects are generally larger in extrastriate areas like V4 than in early visual cortex (Kastner et al., 1999
; McMains and Somers, 2004
). The proposal by Gilbert and colleagues (Li et al., 2004
; Gilbert and Sigman, 2007
) extends the interface hypothesis by including top-down processes other than attention, such as task set, suggesting that a single area and neuron may perform many different functions depending on the demands of the current behavioral task. The interface hypothesis may help resolve the ongoing debate about the role of attentional modulation in primary visual cortex. Isolated stimuli placed in the RFs of V1 neurons often fail to be modulated by attention (McAdams and Maunsell, 1999
), whereas attention to complex stimuli that provide a contextual framework results in modulation of V1 RFs (Motter, 1993
; Ito and Gilbert, 1999
). The interface hypothesis would predict this discrepancy, arguing that only when V1 neurons are engaged as part of a local network, such as the neural circuit representing contextual information, would attentional modulation be large.
The current findings extend the biased competition theory of attention, suggesting that top-down attention is constrained by the output of bottom-up processes, such that the degree of attentional modulation varies monotonically with the degree of competition left unresolved after bottom-up grouping processes have occurred. The interaction of top-down and bottom-up processes provides a mechanism by which attention can select low-salient, but task-relevant stimuli. In addition, the finding that the degree of attentional modulation is inversely related to the output of bottom-up processes challenges the traditional spotlight view of attention, which argues that all task-relevant stimuli within the attentional spotlight will be similarly enhanced, regardless of any distractor or contextual stimuli located outside of the spotlight. Alternatively, the inverse relationship between attention and perceptual grouping can be interpreted within the interface hypothesis originally proposed to explain the relationship between figure–ground processes and attention (Qiu et al., 2007
). The current results extend the interface hypothesis by providing an example of an interface at a different level of processing on which attention can operate, the network containing V4 involved in competitive processes. Together, converging evidence amounts to suggest that attention may operate on several different interfaces that can be recruited at different levels of processing.