Abstract
Perceiving, recognizing and remembering 3-dimensional (3-D) objects encountered in the environment has a very high survival value; unsurprisingly, this ability is shared among many animal species, including humans. The psychological, psychophysical and neural basis for object perception, discrimination, recognition and memory has been extensively studied in humans, monkeys, pigeons and rodents, but is still far from understood. Nearly all 3-D object recognition studies in the rodent used the “novel object recognition” paradigm, which relies on innate rather than learned behavior; however, this procedure has several important limitations. Recently, investigators have begun to recognize the power of behavioral tasks learned through reinforcement training (operant conditioning) to reveal the sensorimotor and cognitive abilities of mice and to elucidate their underlying neural mechanisms. Here, we describe a novel method for training and testing mice in visual and tactile object discrimination, recognition and memory, and use it to begin to examine the underlying sensory basis for these cognitive capacities. A custom-designed Y maze was used to train mice to associate one of two 3-D objects with a food reward. Out of nine mice trained in two cohorts, seven reached performance criterion in about 20–35 daily sessions of 20 trials each. The learned association was retained, or rapidly re-acquired, after a 6 weeks hiatus in training. When tested under low light conditions, individual animals differed in the degree to which they used tactile or visual cues to identify the objects. Switching to total darkness resulted only in a transient dip in performance, as did subsequent trimming of all large whiskers (macrovibrissae). Additional removal of the small whiskers (microvibrissae) did not degrade performance, but transiently increased the time spent inspecting the object. This novel method can be combined in future studies with the large arsenal of genetic tools available in the mouse, to elucidate the neural basis of object perception, recognition and memory.
Highlights
IntroductionThe uncanny ability of humans and other primates to recognize a familiar 3-dimensional (3-D) object by vision or by touch in less than two tenths of a second (Thorpe et al, 1996; Hung et al, 2005; Liu et al, 2009; Gurtubay-Antolin et al, 2015), regardless of lighting, viewing angle, distance or other changing conditions, has long fascinated philosophers, psychologists, computerTraining Mice in Object Discrimination scientists, and both experimental and computational neuroscientists (Bulthoff and Edelman, 1992; Logothetis and Sheinberg, 1996; Tarr and Bulthoff, 1998; Riesenhuber and Poggio, 2002; Palmeri and Gauthier, 2004; Serre et al, 2007; Hoffman and Logothetis, 2009; Ungerleider and Bell, 2011; DiCarlo et al, 2012)
Using operant conditioning and a custom-designed Y maze, we trained mice to discriminate between two objects, a cube and a tetrahedron
Four of the five mice reached our earlier performance criterion, of ≥75% correct trials for three sessions in a row, by the 19th, 21st, 22nd, and 23rd sessions, respectively (Figure 2, left panel); a fifth animal failed to reach this criterion within this training period
Summary
The uncanny ability of humans and other primates to recognize a familiar 3-dimensional (3-D) object by vision or by touch in less than two tenths of a second (Thorpe et al, 1996; Hung et al, 2005; Liu et al, 2009; Gurtubay-Antolin et al, 2015), regardless of lighting, viewing angle, distance or other changing conditions, has long fascinated philosophers, psychologists, computerTraining Mice in Object Discrimination scientists, and both experimental and computational neuroscientists (Bulthoff and Edelman, 1992; Logothetis and Sheinberg, 1996; Tarr and Bulthoff, 1998; Riesenhuber and Poggio, 2002; Palmeri and Gauthier, 2004; Serre et al, 2007; Hoffman and Logothetis, 2009; Ungerleider and Bell, 2011; DiCarlo et al, 2012). A common object recognition paradigm, used in primate studies for over half a century, is the “Delayed Match/Non-Match to Sample” (DMS/DNMS) test (Mishkin et al, 1962; Mishkin and Delacour, 1975; Zola-Morgan et al, 1989). In this procedure an object is first presented to the animal for sampling and, after a variable delay, presented again together with a different object. While superficially similar to the DNMS paradigm, in the NOR test the animal is not trained; rather, the experiment relies on the natural tendency of rodents (and other species) to spend more time exploring a novel object in preference to a previously encountered one (reviewed in Dere et al, 2007; Winters et al, 2008; Antunes and Biala, 2012; Blaser and Heyser, 2015)
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