Elsevier

Behavioural Brain Research

Volume 285, 15 May 2015, Pages 118-130
Behavioural Brain Research

Review
The neural bases of crossmodal object recognition in non-human primates and rodents: A review

https://doi.org/10.1016/j.bbr.2014.09.039Get rights and content

Highlights

  • Multisensory integration (MSI) is essential to everyday behavior.

  • The neural substrates of MSI are poorly understood.

  • We review non-human studies of MSI using crossmodal object recognition tasks.

  • This research reveals roles for various cortical regions and neurochemical systems.

Abstract

The ability to integrate information from different sensory modalities to form unique multisensory object representations is a highly adaptive cognitive function. Surprisingly, non-human animal studies of the neural substrates of this form of multisensory integration have been somewhat sparse until very recently, and this may be due in part to a relative paucity of viable testing methods. Here we review the historical development and use of various “crossmodal” cognition tasks for non-human primates and rodents, focusing on tests of “crossmodal object recognition”, the ability to recognize an object across sensory modalities. Such procedures have great potential to elucidate the cognitive and neural bases of object representation as it pertains to perception and memory. Indeed, these studies have revealed roles in crossmodal cognition for various brain regions (e.g., prefrontal and temporal cortices) and neurochemical systems (e.g., acetylcholine). A recent increase in behavioral and physiological studies of crossmodal cognition in rodents augurs well for the future of this research area, which should provide essential information about the basic mechanisms of object representation in the brain, in addition to fostering a better understanding of the causes of, and potential treatments for, cognitive deficits in human diseases characterized by atypical multisensory integration.

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.

References (193)

  • J.A. Tomie et al.

    New paradigms for tactile discrimination studies with the rat: methods for simple, conditional, and configural discriminations

    Physiol Behav

    (1990)
  • A. Ennaceur et al.

    A new one-trial test for neurobiological studies of memory in rats. 1: Behavioral data

    Behav Brain Res

    (1988)
  • J.M. Reid et al.

    Crossmodal object recognition in rats with and without multimodal object pre-exposure: no effect of hippocampal lesions

    Neurobiol Learn Mem

    (2012)
  • H.B.M. Uylings et al.

    Do rats have a prefrontal cortex

    Behav Brain Res

    (2003)
  • P.G. Aitken

    Lesion effects on tactual to visual cross-modal matching in the rhesus monkey

    Neuropsychologia

    (1980)
  • G. Ettlinger et al.

    Cross-modal recognition by the monkey: the effects of cortical removals

    Neuropsychologia

    (1980)
  • P. Lipton et al.

    Crossmodal associative memory representations in rodent orbitofrontal cortex

    Neuron

    (1999)
  • M. Fenske et al.

    Top-down faciltation of visual object recognition: object-based and context-based contributions

    Prog Brain Res

    (2006)
  • W. Hörster et al.

    The neural structures involved in cross-modal recognition and tactile discrimination performance: an investigation using 2-DG

    Behav Brain Res

    (1989)
  • G. Ettlinger et al.

    Cross-modal performance: behavioural processes, phylogenetic considerations and neural mechanisms

    Behav Brain Res

    (1990)
  • J.P. Aggleton

    Understanding retrosplenial amnesia: insights from animal studies

    Neuropsychologia

    (2010)
  • R.L. Reep et al.

    Posterior parietal cortex as part of a neural network for directed attention in rats

    Neurobiol Learn Mem

    (2009)
  • R. Tees

    The effects of posterior parietal and posterior temporal cortical lesions on mulitmodal spatail and nonspatial competencies in rats

    Behav Brain Res

    (1999)
  • M. Streicher et al.

    Cross-modal recognition and unfamilar objects by the monkey: the effects of ablation of polysensory neocortex or of the amygdaloid complex

    Behav Brain Res

    (1987)
  • A. Parker et al.

    Lesions of the primate rhinal cortex cause deficits in flavour-visual associative memory

    Behav Brain Res

    (1998)
  • M.J. Buckley et al.

    Perirhinal cortical contributions to object perception

    Trends Cogn Sci

    (2006)
  • M.D. Barense et al.

    The human medial temporal lobe processes online representations of complex objects

    Neuropsychologia

    (2007)
  • H.H. Wylie

    An experimental study of transfer of response in the white rat

    Behav Monogr

    (1919)
  • G. Ettlinger

    Cross-modal transfer of training in monkeys

    Behaviour

    (1960)
  • L.C. Botly et al.

    Cholinergic influences on feature binding

    Behav Neurosci

    (2007)
  • L.C. Botly et al.

    Cholinergic deafferentation of the neocortex using 192 IgG-saporin impairs feature binding in rats

    J Neurosci

    (2009)
  • L.C. Botly et al.

    A cross-species investigation of acetylcholine, attention, and feature binding

    Psychol Sci

    (2008)
  • B.D. Winters et al.

    A distributed cortical representation underlies crossmodal object recognition in rats

    J Neurosci

    (2010)
  • J.M. Reid et al.

    Delineating prefrontal cortex region contributions to crossmodal object recognition in rats

    Cereb Cortex

    (2013)
  • L.S. Stepien et al.

    Memory in monkeys for compound stimuli

    Am J Psychol

    (1960)
  • D. Burton et al.

    Cross-modal transfer of training in monkeys

    Nature

    (1960)
  • J.G. Wegener

    Cross-modal transfer in monkeys

    J Comp Physiol Psychol

    (1965)
  • G. Ettlinger et al.

    Cross-modal transfer of conditional discrimination training in monkeys

    Nature

    (1966)
  • M. Wilson et al.

    Intersensory facilitation of learning sets in normal and brain operated monkeys

    J Comp Physiol Psychol

    (1962)
  • M. Wilson

    Further analysis of intersensory facilitation of learning sets in monkeys

    Percept Mot Skills

    (1964)
  • W.A. Wilson et al.

    Intermodality transfer of specific discriminations in the monkey

    Nature

    (1963)
  • R.K. Davenport et al.

    Intermodal equivalence of stimuli in apes

    Science (New York, NY)

    (1970)
  • R.K. Davenport et al.

    Perception of photographs by apes

    Behaviour

    (1971)
  • G.H. Bower

    Analysis of a mnemonic device: modern psychology uncovers the powerful components of an ancient system for improving memory

    Am Sci

    (1970)
  • M. Petrides et al.

    Cross-modal matching and the primate frontal cortex

    Science

    (1976)
  • E. Murray et al.

    Cross-modal associations, intramodal associations and object identification in macaque monkeys

  • R.B. Bolster

    Cross-modal matching in the monkey (Macaca fascicularis)

    Neuropsychologia

    (1978)
  • E.A. Murray et al.

    Amygdalectomy impairs crossmodal association in monkeys

    Science

    (1985)
  • Murray EA, Bussey TJ, Hampton RR, Saksida LM. The parahippocampal region and object identification. Prepared for M....
  • M. Colombo et al.

    Effects of auditory and visual interference on auditory-visual delayed matching to sample in monkeys (Macaca fascicularis)

    Behav Neurosci

    (1994)
  • Cited by (17)

    • Performance of the odour span task is not impaired following inactivations of parietal cortex in rats

      2018, Behavioural Brain Research
      Citation Excerpt :

      We used CMOR as a positive control to verify that our inactivations sufficiently disrupted PC function. This task assesses the ability of rats to use multisensory integration to recognize objects [22–25], and relies in part on the PC [23]. The present findings showed an impairment in the cross-modal phase of CMOR after inactivations of the PC, in line with previous findings [23], and confirm the efficacy of our inactivations.

    • Exploiting Novelty and Oddity Exploratory Preferences in Rodents to Study Multisensory Object Memory and Perception

      2018, Handbook of Behavioral Neuroscience
      Citation Excerpt :

      The sample phase ends when the rat accumulates 25 s of object exploration or after 3 min has elapsed. Following the sample phase, rats are placed in the start arm of the Y-apparatus or returned to their home cage for a retention delay that can vary anywhere between 15 s and 1 h (Winters and Reid, 2010; Reid et al., 2012; Jacklin et al. 2012, 2016; Cloke et al. 2015, 2016); rats struggle to perform the CMOR task with delays greater than 1h unless additional manipulations are performed (see below). To shorten the retention delay below 30 s in order to minimize the mnemonic demand, objects can be placed on top of inserts for quicker removal and immediate choice phase object presentation (see Figure 1 in Cloke and Winters, 2015).

    • Variants of the Spontaneous Recognition Procedure Assessing Multisensory Integration Reveal Behavioral Alterations in Rodent Models of Psychiatric and Neurological Disorders

      2018, Handbook of Behavioral Neuroscience
      Citation Excerpt :

      Although an exact network of CMOR has not been established, a number of cortical and subcortical areas receiving convergent projections from different sensory regions have been identified. These include the premotor, perirhinal, anterior cingulate, and prefrontal cortices within the cortex and the hippocampus, claustrum, and superior colliculus, located subcortically (Cloke et al., 2015). The simultaneous oddity discrimination task was developed to assess perceptual processing while circumventing the mnemonic demands required for typical SOR tasks (Bartko et al., 2007a).

    • Tactile information improves visual object discrimination in kea, Nestor notabilis, and capuchin monkeys, Sapajus spp.

      2018, Animal Behaviour
      Citation Excerpt :

      Thus, although the object discrimination was performed only using the visual modality in both experimental conditions, it is reasonable to assume that in the Sight and Touch condition the retrieval of the stored tactile information supported discrimination processes in the visual modality. Hence, our study revealed that visuotactile integration can enhance the subsequent unisensory visual recognition and it expands on previous findings demonstrating cross-modal transfer of information between sight and touch in nonhuman species (e.g. Cowey & Weiskrantz, 1975; Davenport & Rogers, 1970; Elliott, 1977; Petrides & Iversen, 1976; Reid et al., 2012, 2013; Weiskrantz & Cowey, 1975; Winters & Reid, 2010; for a review see Cloke et al., 2015). A further comment should be made on the implications of the procedure we used.

    • Perirhinal Cortex: Neural Representations

      2017, Learning and Memory: A Comprehensive Reference
    View all citing articles on Scopus
    View full text