ReviewThe neural bases of crossmodal object recognition in non-human primates and rodents: A review
Introduction
At any given moment, our brains are inundated with stimuli arriving through distinct, highly specialized sensory channels. Despite the relative segregation of early sensory pathways in the brain, our experience of and interactions with the outside world are shaped by multimodal constructs resulting from the integration of information across sensory systems. Although seemingly effortless, the importance of multisensory integration is likely derived from the adaptive value conferred upon recognition processes. For instance, when faced with the potential presence of a predator, the ability to rapidly select the appropriate behavioral response relies on an efficient assessment of the situation. It is often in these circumstances that visual information alone is not sufficient to adequately guide behavior, as lighting may be poor or the predator obscured from view. Therefore, accurate recognition of a potential threat would be greatly enhanced by the amalgamation of sensory stimuli which in isolation may not sufficiently evoke concern, but when integrated would indicate the presence of an imminent danger.
This is just one example of the influence that multisensory object representation can have over behavior. In many subtler ways, our ongoing behavior is driven by our reactions to the multisensory features of the everyday objects we encounter. Moreover, it is becoming increasing apparent that various human cognitive disorders (e.g., schizophrenia, autism, Alzheimer's disease) are associated with atypical multisensory integration abilities. Considering the adaptive behavioral influence of multisensory integration, these deficits could be at the root of many of the other cognitive symptoms displayed by patients with these conditions, and a better understanding of multisensory brain mechanisms could reveal novel insight into basic object representation functions, as well as strategies for treating cognitive impairment.
The current review will focus on a relatively neglected area of multisensory research, the use of non-human primates and rodents to study “crossmodal object recognition”, or the ability to recognize objects across sensory modalities. Despite receiving substantial interest from behavioral neuroscientists in the 1960s, 1970s, and 1980s, work in this area trailed off for several years. However, crossmodal object recognition research appears to be gaining traction once again with the recent development of novel rodent tests that have clearly been influenced by the earlier, predominantly non-human primate, paradigms. This is a promising development given the relative ease with which such tasks can be applied to non-human studies, which remain an important source of information about the neurobiological bases of behavior. This work has great potential to help uncover the neural substrates of complex object representation, as well as helping to better characterize mechanisms of multisensory integration, which is relevant to many vital cognitive functions, such as attention, emotion, perception, learning, and memory. We will first review the historical development of crossmodal object recognition tasks for non-human primates and rodents. Next, we will survey the literature regarding the neurobiological bases of performance in these tasks. Finally, we will discuss the relevance of crossmodal object recognition tasks to human cognitive disorders.
Section snippets
Development of crossmodal object recognition tasks for non-human primates
Early work on crossmodal cognition originated from studies exploring crossmodal transfer of responses. In such tasks, learning in one modality is aided by previous learning of a similar task in a different modality. In one such study, rats learned to produce a habitual motoric behavior in the presence of either an auditory or visual stimulus. Reward was contingent upon returning to a feeding area via one of two return alleys. Once a return alley was selected, rats were required to change
Development of crossmodal object recognition tasks for rodents
Given the difficulty associated with developing crossmodal object recognition tasks for non-human primates, it is unsurprising that, until recently, few attempts were made to establish a rodent analog. Following the early work of Wylie [1], Over and Mackintosh [34] assessed crossmodal transfer in rats using an audio-visual discrimination task. Rats were trained in an operant chamber to discriminate between high and low intensities of either a sound or a light. Responding on a lever during
Prefrontal cortex
The development of a successful crossmodal object recognition task by Cowey and Weiskrantz [23] precipitated the investigation of the neural underpinnings of crossmodal processing in non-human primates. The prefrontal cortex (PFC) is known to be a convergence site of multiple sensory inputs, suggesting its participation in crossmodal task performance [44], [45], [46], [47]. Early studies demonstrated that bilateral ablation of the arcuate sulcus or anterior cingulate cortex of the PFC in
Clinical relevance of this research
Many human disorders associated with cognitive impairment – including Alzheimer's disease (AD), autism, and schizophrenia (Sz) – count atypical multisensory integration amongst their symptoms, yet this cognitive function remains relatively understudied in patients and preclinical animal models. We have recently made inroads in this area by applying the CMOR task to the investigation of multisensory impairment in an established rat model of schizophrenia [131].
Conclusions and future directions
In all, there has been an encouraging recent increase in the number of studies investigating crossmodal object recognition and multisensory integration in rodents and non-human primates. By modifying, adapting, and elaborating on the paradigms developed by early researchers, this work has great potential to influence thinking about the way the mammalian brain represents objects, a better understanding of which could also facilitate better treatments for certain forms of cognitive dysfunction.
Acknowledgements
This work was supported by a Discovery Grant from the Natural Sciences and Engineering Research Council of Canada (NSERC) (400176) to BDW, as well as an NSERC post-graduate scholarship to JMC and an Ontario Graduate Scholarship to DLJ.
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