The Dynamic Multisensory Engram: Neural Circuitry Underlying Crossmodal Object Recognition in Rats Changes with the Nature of Object Experience

Abstract

Rats, humans, and monkeys demonstrate robust crossmodal object recognition (CMOR), identifying objects across sensory modalities. We have shown that rats' performance of a spontaneous tactile-to-visual CMOR task requires functional integration of perirhinal (PRh) and posterior parietal (PPC) cortices, which seemingly provide visual and tactile object feature processing, respectively. However, research with primates has suggested that PRh is sufficient for multisensory object representation. We tested this hypothesis in rats using a modification of the CMOR task in which multimodal preexposure to the to-be-remembered objects significantly facilitates performance. In the original CMOR task, with no preexposure, reversible lesions of PRh or PPC produced patterns of impairment consistent with modality-specific contributions. Conversely, in the CMOR task with preexposure, PPC lesions had no effect, whereas PRh involvement was robust, proving necessary for phases of the task that did not require PRh activity when rats did not have preexposure; this pattern was supported by results from c-fos imaging. We suggest that multimodal preexposure alters the circuitry responsible for object recognition, in this case obviating the need for PPC contributions and expanding PRh involvement, consistent with the polymodal nature of PRh connections and results from primates indicating a key role for PRh in multisensory object representation. These findings have significant implications for our understanding of multisensory information processing, suggesting that the nature of an individual's past experience with an object strongly determines the brain circuitry involved in representing that object's multisensory features in memory.

Medial prefrontal-perirhinal cortical communication is necessary for flexible response selection

“…Synaptic weight changes within the PER support associations between object pairs (Fujimichi, Naya, Koyano, Takeda, Takeuchi, and Miyashita, 2010; Higuchi and Miyashita, 1996; Murray and Richmond, 2001), and it is conceivable that this could extend across modalities. In fact, the PER is critical for linking visual to tactile information (Buckley and Gaffan, 1998a; Goulet and Murray, 2001; Jacklin, Cloke, Potvin, Garrett, and Winters, 2016; Parker and Gaffan, 1998; Reid, Jacklin, and Winters, 2014). A similar situation may occur when an object is associated with a place.…”

Cross-Talk of Low-Level Sensory and High-Level Cognitive Processing: Development, Mechanisms, and Relevance for Cross-Modal Abilities of the Brain

“…Experimental research examining the mechanisms of sensory convergence in low-level sensory regions emphasized the processing and relay of basic object feature information (Iurilli et al, 2012;Sieben et al, 2013;Bieler et al, 2018;Morrill and Hasenstaub, 2018). However, the formation, storage, and utilization of cross-modal object representations during behavior require an interaction of neuronal areas accounting for sensory and cognitive processing (Hindley et al, 2014;Reid et al, 2014;Jacklin et al, 2016). Thus, while both sensory integration and separation are part of bottom-up crossmodal processing in primary sensory cortices, the mechanisms underlying the functional communication between low-and high-level brain areas during cross-modal perception are still largely unknown.…”

“…Furthermore, top-down modulation reweights sensory information and facilitates the integration of cross-modal inputs (Alsius et al, 2005;Busse et al, 2005;Bresciani and Ernst, 2007;Talsma et al, 2007;Lakatos et al, 2009;Fiebelkorn et al, 2010;Muhlberg et al, 2014). Prior crossmodal exploration of task-relevant objects significantly facilitates the detection performance of a rat in a cross-modal object recognition task (Jacklin et al, 2016). Moreover, rats are able to recognize a visually presented object, which has been only explored by the tactile sense (Winters and Reid, 2010).…”

Feedback inhibition derived from the posterior parietal cortex regulates the neural properties of the mouse visual cortex

“…Feedback from the higher association areas is thought to have very important roles in the cortical processing of sensory information (Gilbert & Li, ; Hochstein & Ahissar, ; Lamme & Roelfsema, ; Petro, Vizioli, & Muckli, ), but it is poorly understood how the information processed in higher association areas regulates functions of the primary sensory areas. Accumulating evidence shows that feedback modulations may be important for higher cognitive abilities such as multimodal integration (Grefkes & Fink, ; Jacklin, Cloke, Potvin, Garrett, & Winters, ) and attentional control (Ruff, ; Schiffino, Zhou, & Holland, ). However, it remains uncertain how the feedback modulations work to achieve these higher functions.…”