Laura Cacciamani

The perirhinal cortex modulates V2 activity in response to the agreement between part familiarity and configuration familiarity

Research has demonstrated that the perirhinal cortex (PRC) represents complex object‐level feature configurations, and participates in familiarity versus novelty discrimination. Barense et al. [(in press) Cerebral Cortex, 22:11, doi:10.1093/cercor/bhr347] postulated that, in addition, the PRC modulates part familiarity responses in lower‐level visual areas. We used fMRI to measure activation in the PRC and V2 in response to silhouettes presented peripherally while participants maintained central fixation and performed an object recognition task. There were three types of silhouettes: Familiar Configurations portrayed real‐world objects; Part‐Rearranged Novel Configurations created by spatially rearranging the parts of the familiar configurations; and Control Novel Configurations in which both the configuration and the ensemble of parts comprising it were novel. For right visual field (RVF) presentation, BOLD responses revealed a significant linear trend in bilateral BA 35 of the PRC (highest activation for Familiar Configurations, lowest for Part‐Rearranged Novel Configurations, with Control Novel Configurations in between). For left visual field (LVF) presentation, a significant linear trend was found in a different area (bilateral BA 38, temporal pole) in the opposite direction (Part‐Rearranged Novel Configurations highest, Familiar Configurations lowest). These data confirm that the PRC is sensitive to the agreement in familiarity between the configuration level and the part level. As predicted, V2 activation mimicked that of the PRC: for RVF presentation, activity in V2 was significantly higher in the left hemisphere for Familiar Configurations than for Part‐Rearranged Novel Configurations, and for LVF presentation, the opposite effect was found in right hemisphere V2. We attribute these patterns in V2 to feedback from the PRC because receptive fields in V2 encompass parts but not configurations. These results reveal two new aspects of PRC function: (1) it is sensitive to the congruency between the familiarity of object configurations and the parts comprising those configurations and (2) it likely modulates familiarity responses in visual area V2.

Competition-strength-dependent ground suppression in figure–ground perception

Figure–ground segregation is modeled as inhibitory competition between objects that might be perceived on opposite sides of borders. The winner is the figure; the loser is suppressed, and its location is perceived as shapeless ground. Evidence of ground suppression would support inhibitory competition models and would contribute to explaining why grounds are shapeless near borders shared with figures, yet such evidence is scarce. We manipulated whether competition from potential objects on the ground side of figures was high (i.e., portions of familiar objects were potentially present there) or low (novel objects were potentially present). We predicted that greater competition would produce more ground suppression. The results of two experiments in which suppression was assessed via judgments of the orientation of target bars confirmed this prediction; a third experiment showed that ground suppression is short-lived. Our findings support inhibitory competition models of figure assignment, in particular, and models of visual perception entailing feedback, in general.

Toward a Dynamical View of Object Perception

We review our research demonstrating that object perception is a dynamical, integrated process in which (a) high-level memory representations are accessed before objects are perceived; (b) potential objects compete for perception and only the winners are perceived; and (c) there is no clear dividing line between perception and memory. We begin by describing the results that originally led us to reject the traditional serial hierarchical view of object perception as well as modern feedforward models. We then summarize the accumulating evidence that led us to favor a more dynamical model involving feedback as well as feedforward processing and interactions between high- and low-levels of the visual hierarchy. Throughout, we highlight how our views changed over time.

Semantic access occurs outside of awareness for the ground side of a figure

Traditional theories of vision assume that figures and grounds are assigned early in processing, with semantics being accessed later and only by figures, not by grounds. We tested this assumption by showing observers novel silhouettes with borders that suggested familiar objects on their ground side. The ground appeared shapeless near the figure’s borders; the familiar objects suggested there were not consciously perceived. Participants’ task was to categorize words shown immediately after the silhouettes as naming natural versus artificial objects. The words named objects from the same or from a different superordinate category as the familiar objects suggested in the silhouette ground. In Experiment 1, participants categorized words faster when they followed silhouettes suggesting upright familiar objects from the same rather than a different category on their ground sides, whereas no category differences were observed for inverted silhouettes. This is the first study to show unequivocally that, contrary to traditional assumptions, semantics are accessed for objects that might be perceived on the side of a border that will ultimately be perceived as a shapeless ground. Moreover, although the competition for figural status results in suppression of the shape of the losing contender, its semantics are not suppressed. In Experiment 2, we used longer silhouette-to-word stimulus onset asynchronies to test whether semantics would be suppressed later in time, as might occur if semantics were accessed later than shape memories. No evidence of semantic suppression was observed; indeed, semantic activation of the objects suggested on the ground side of a border appeared to be short-lived. Implications for feedforward versus dynamical interactive theories of object perception are discussed.

Spatially rearranged object parts can facilitate perception of intact whole objects

The familiarity of an object depends on the spatial arrangement of its parts; when the parts are spatially rearranged, they form a novel, unrecognizable configuration. Yet the same collection of parts comprises both the familiar and novel configuration. Is it possible that the collection of familiar parts activates a representation of the intact familiar configuration even when they are spatially rearranged? We presented novel configurations as primes before test displays that assayed effects on figure-ground perception from memories of intact familiar objects. In our test displays, two equal-area regions shared a central border; one region depicted a portion of a familiar object. Previous research with such displays has shown that participants are more likely to perceive the region depicting a familiar object as the figure and the abutting region as its ground when the familiar object is depicted in its upright orientation rather than upside down. The novel primes comprised either the same or a different collection of parts as the familiar object in the test display (part-rearranged and control primes, respectively). We found that participants were more likely to perceive the familiar region as figure in upright vs. inverted displays following part-rearranged primes but not control primes. Thus, priming with a novel configuration comprising the same familiar parts as the upcoming figure-ground display facilitated orientation-dependent effects of object memories on figure assignment. Similar results were obtained when the spatially rearranged collection of parts was suggested on the groundside of the primes border, suggesting that familiar parts in novel configurations access the representation of their corresponding intact whole object before figure assignment. These data demonstrate that familiar parts access memories of familiar objects even when they are arranged in a novel configuration.

Memory-guided drawing training increases Granger causal influences from the perirhinal cortex to V1 in the blind

HIGHLIGHTSThe proposal that the perirhinal cortex (PRC) modulates V1 in the blind was tested.FMRI scans were conducted before and after Cognitive‐Kinesthetic drawing training.The training led to enhanced top‐down Granger causal influences from the PRC to V1.Results suggest that the PRC is a potential source of V1 reorganization in the blind. ABSTRACT The perirhinal cortex (PRC) is a medial temporal lobe structure that has been implicated in not only visual memory in the sighted, but also tactile memory in the blind (Cacciamani & Likova, 2016). It has been proposed that, in the blind, the PRC may contribute to modulation of tactile memory responses that emerge in low‐level “visual” area V1 as a result of training‐induced cortical reorganization (Likova, 2012, 2015). While some studies in the sighted have indicated that the PRC is indeed structurally and functionally connected to the visual cortex (Clavagnier, Falchier, & Kennedy, 2004; Peterson, Cacciamani, Barense, & Scalf, 2012), the PRCs direct modulation of V1 is unknown—particularly in those who lack the visual input that typically stimulates this region. In the present study, we tested Likovas PRC modulation hypothesis; specifically, we used fMRI to assess the PRCs Granger causal influence on V1 activation in the blind during a tactile memory task. To do so, we trained congenital and acquired blind participants on a unique memory‐guided drawing technique previously shown to result in V1 reorganization towards tactile memory representations (Likova, 2012). The tasks (20 s each) included: tactile exploration of raised line drawings of faces and objects, tactile memory retrieval via drawing, and a scribble motor/memory control. FMRI before and after a week of the Cognitive‐Kinesthetic training on these tasks revealed a significant increase in PRC‐to‐V1 Granger causality from pre‐ to post‐training during the memory drawing task, but not during the motor/memory control. This increase in causal connectivity indicates that the training strengthened the top‐down modulation of visual cortex from the PRC. This is the first study to demonstrate enhanced directed functional connectivity from the PRC to the visual cortex in the blind, implicating the PRC as a potential source of the reorganization towards tactile representations that occurs in V1 in the blind brain (Likova, 2012).

Tactile Object Familiarity in the Blind Brain Reveals the Supramodal Perceptual-Mnemonic Nature of the Perirhinal Cortex

This study is the first to investigate the neural underpinnings of tactile object familiarity in the blind during both perception and memory. In the sighted, the perirhinal cortex (PRC) has been implicated in the assessment of visual object familiarity—a crucial everyday task—as evidenced by reduced activation when an object becomes familiar. Here, to examine the PRC’s role in tactile object familiarity in the absence of vision, we trained blind participants on a unique memory-guided drawing technique and measured brain activity while they perceptually explored raised-line drawings, drew them from tactile memory, and scribbled (control). Functional magnetic resonance imaging (fMRI) before and after a week of training revealed a significant decrease in PRC activation from pre- to post-training (i.e., from unfamiliar to familiar) during perceptual exploration as well as memory-guided drawing, but not scribbling. This familiarity-based reduction is the first evidence that the PRC represents tactile object familiarity in the blind. Furthermore, the finding of this effect during both tactile perception and tactile memory provides the critical link in establishing the PRC as a structure whose representations are supramodal for both perception and memory.

Accessing meaning for the groundside of a figure: How long does it last?

• Consistent with view that potential objects on opposite sides of borders are processed to high levels in a first pass of processing • Figure-ground perception entails inhibitory competition between possible objects on opposite sides of a border • Previous study[1]: Are the semantics of the competing objects accessed before figure assignment? • Strategy: Assess whether semantics of loser are accessed • Task: categorize words as naming natural/artificial objects • Words followed silhouettes with real-world, familiar shapes suggested but not perceived on the groundside • 83 ms silhouette-to-word SOA

Competition-based ground suppression in extrastriate cortex and the role of attention

1. Duncan & Desimone (1995). Ann rev neurosci, 18(1), 193-222. 2. Beck & Kastner (2009). Vis Rsrch, 49(10), 1154-1165 3. Jehee, Lamme, & Roelfsema (2007). Vis Rsrch, 47, 1153-1165. 4. Vecera & O’Reilly (1998). JEP:HPP, 24, 441-462. 5. Peterson & Skow (2008). JEP:HPP, 34, 251-267. 6. Salvagio, Cacciamani, & Peterson (2012). AP&P, 74, 964-978. Neural evidence of ground suppression arising from objectlevel inhibitory competition • Greater competition from high-competition ground in V4 where RFs are large (~4o) • Greater ground suppression in V4 for High-C than Low-C