Object identification leads to a conceptual broadening of object representations in lateral prefrontal cortex

Abstract

Recent experience identifying objects leads to later improvements in both speed and accuracy (“repetition priming”), along with simultaneous reductions of neural activity (“repetition suppression”). A popular interpretation of these joint behavioral and neural phenomena is that object representations become perceptually “sharper” with stimulus repetition, eliminating cells that are poorly stimulus-selective and responsive and reducing support for competing representations downstream. Here, we test this hypothesis in an fMRI-adaptation experiment using pictures of objects. Prior to fMRI, participants repeatedly named a set of object pictures. During fMRI, participants viewed adaptation sequences composed of rapidly repeated objects (3-6 repetitions over several seconds) that were either named previously or that were new for the fMRI session, followed by single “deviant” object pictures used to measure recovery from adaptation and that shared a relationship to the adapted picture (a different exemplar of the same object, a conceptual associate, or an unrelated picture). Effects of adaptation and recovery were found throughout visually responsive brain regions. Occipitotemporal cortical regions displayed repetition suppression to previously named relative to new adaptors but failed to exhibit pronounced changes in neural tuning. In contrast, changes in the slope of the recovery curves were found in the left lateral prefrontal cortex: Greater residual adaptation was observed to exemplar stimuli and conceptual associates following previously named adapting stimuli, consistent with greater rather than reduced neural overlap among representations of conceptually related objects. Furthermore, this change in neural tuning was directly related to the proportion of conceptual errors made by participants in the naming sessions pre- and post-fMRI, establishing that the experience-dependent conceptual broadening of object representations seen in fMRI is also manifest in behavior. In a follow-up behavioral experiment, we further show that recent naming experience leads to greater semantic priming when using the previously named pictures as briefly presented primes. Taken together, our results fail to support perceptual sharpening as the primary mediator between repetition suppression and behavioral priming at durations typically used to study priming and instead highlight an experience-dependent broadening of conceptual representations. We suggest that alternative mechanisms, such as increases in neural synchronization, are more promising in explaining priming in the face of repetition suppression.

Incremental learning of perceptual and conceptual representations and the puzzle of neural repetition suppression

“…Challenges to incremental learning posed by Gotts et al (2014) Taken together, the results from our study appear to present two basic challenges to incremental learning models. The first is that after a relatively small number of stimulus repetitions, activity decreases occur in the occipitotemporal cortex without much concomitant change in neural tuning.…”

“…However, it seems clear that over the course of additional training, this should eventually give way to the model utilizing distinctive features at the expense of shared features (as in the current Oppenheim et al model), eliminating the activation of inappropriate related names and ultimately decreasing conceptual relatedness effects (e.g., see later epochs in Simulations 3 and 5 in Rogers & McClelland, 2004). Perhaps this would also have been seen experimentally in the task used by Gotts et al (2014) if greater than five repetitions had been used prior to fMRI. A related possibility is that the tuning changes accompanying picture naming are interacting with the existing structure of perceptual and conceptual representations, with changes that -while conceptual -are less strong than they would have been under a task such as categorization.…”

“…One might also expect that these contexts would have more ecological validity, since they are more in line with what people typically encounter when interacting with objects intermittently in the environment or with their corresponding names in print. As mentioned in the previous section, these challenging effects are twofold: (1) there is a notable lack of evidence of perceptual sharpening over a small number of repetitions (e.g., De Baene & Vogels, 2010;Gotts et al, 2014;Li et al, 1993;McMahon & Olson, 2007;Miller et al, 1993;Weiner et al, 2010), and (2) there is evidence of an expansion of conceptual representations in picture naming in contrast to the apparent task demands for perceptual sharpening (e.g., Gotts et al, 2014;see Gronau, Neta & Bar, 2008, for related results). Incremental learning models might respond to the first challenge by incorporating effects such as spike synchrony (e.g., Friston, 2012), retaining their basic plasticity mechanisms that apply to average firing rate (see Gotts, 2003;Gotts et al, 2012a, for discussion), but how might the second challenge be addressed?…”

“…Repetition priming was also not assessed in any of the above studies, making it difficult to assess the inter-relationships of priming, repetition suppression, and changes in tuning, task-relevant or otherwise. A recent study in our laboratory has directly examined these inter-relationships using fMRI adaptation (Gotts, Milleville, & Martin, 2014). Rather than training subjects to categorize novel objects, we had subjects repeatedly name a large set of well-known objects (e.g., dog, hammer, etc.)…”

“…Over trials, lexical units were activated more rapidly and accurately (repetition priming), but this occurred faster when blocks were composed of unrelated items, since each object suffered less from weakened semantic-> lexical weights involving shared semantic features with other objects in the set (along the lines discussed for the object naming example in the section Incremental learning models: the role of task demands on learned representations). While this model accounts quite nicely for a variety of effects in blocked cyclic naming (e.g., Belke, 2008;Belke, 2008;Damian & Als, 2005;Howard et al, 2006;Hsiao et al, 2009;Navarrete et al, 2014;Schnur et al, 2006), it is less clear how it would address the broadened conceptual representations and enhanced semantic priming observed in Gotts et al (2014). This model should decrease relatedness of conceptual associates by attenuating the impact of shared semantic features on lexical processing over learning.…”