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Developmental Neuroscience of Time and Number: Implications for Autism and Other Neurodevelopmental Disabilities

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Developmental Neuroscience of Time and Number: Implications for Autism and Other Neurodevelopmental Disabilities View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by PubMed Central REVIEW ARTICLE published: 06 March 2012 INTEGRATIVE NEUROSCIENCE doi: 10.3389/fnint.2012.00007 Developmental neuroscience of time and number: implications for autism and other neurodevelopmental disabilities Melissa J. Allman 1*, Kevin A. Pelphrey 2 and Warren H. Meck 3 1 Kennedy Krieger Institute, The Johns Hopkins University School of Medicine, Baltimore, MD, USA 2 Yale Child Study Center, Yale School of Medicine, New Haven, CT, USA 3 Department of Psychology and Neuroscience, Duke University, Durham, NC, USA Edited by: Estimations of time and number share many similarities in both non-humans and man. Valerie Doyere, Centre National de la The primary focus of this review is on the development of time and number sense Recherche Scientifique, France across infancy and childhood, and neuropsychological findings as they relate to time and Reviewed by: number discrimination in infants and adults. Discussion of these findings is couched Catherine Jones, University of Essex, UK within a mode-control model of timing and counting which assumes time and number Mark Yates, University of share a common magnitude representation system. A basic sense of time and number Melbourne, Australia likely serves as the foundation for advanced numerical and temporal competence, and *Correspondence: aspects of higher cognition—this will be discussed as it relates to typical childhood, and Melissa J. Allman, Kennedy Krieger certain developmental disorders, including autism spectrum disorder. Directions for future Institute, The Johns Hopkins University School of Medicine, research in the developmental neuroscience of time and number (NEUTIN) will also be 707 N. Broadway, Baltimore, highlighted. MD, USA. e-mail: [email protected]; Keywords: timing and time perception, temporal cognition, counting, numerical cognition, mode-control models, [email protected] cortico-striatal circuits INTRODUCTION (e.g., Meck and Church, 1983), and those that suppose our abil- The interval timing and numerical abilities identified in non- ity to make sense of time, space, and numerosity develops from human animals, human infants, and children may represent bio- a single magnitude processing system (A Theory of Magnitude, logical and developmental precursors of adults’ highly developed ATOM; Walsh, 2003). In fact, in humans at least, they are most computational abilities (Buhusi and Cordes, 2011; Lustig, 2011; likely component processes in a cognitive system: a “raw sub- Williams, 2011). For instance, at the perceptual level, non-humans strate” magnitude estimate of time and number is likely processed andinfantsappearcapableofmakingmagnitudeestimatesofdura- by some ordinal magnitude comparator (which is recruited to tion, numerosity and area (i.e., that a given stimulus is presented make “how much” or “more than and less than” judgments) that for “more” time than another, or contains “more” elements—this apparently deals with many different dimensions (time, space, basic ability is the focus of our review). The ability to imagine numerosity, loudness and luminance, and even emotional expres- events in the future (which must by implication, require some sion; e.g., see Smith and Sera, 1992; Holmes and Lourenco, 2009). form of internal time sense) has been postulated to be related to Although ATOM assumes that “time and quantity estimation our ability to “anticipate future mental processes and motivational operate on similar and partly shared accumulation principles” of and emotional states” (Pezzulo and Rigoli, 2011:1), and adults at the type described in the mode-control model, these two forms least appear able to comprehend metaphysical and higher concepts of account (Meck and Church, 1983; Walsh, 2003)maybethe- of time and space (e.g., imagining the size of the galaxy, or how oretically dissociated at the developmental level—for instance, long it has been around). It seems parsimonious to suppose that the mode-control model assumes numerosity is the product of the basic ability to represent time, space and numerosity is a basic an internal (primitive) count, which is “built in,” and accord- developmental “building block” for math ability, and abstract ing to ATOM, numerosity is acquired by learning associations mental representations and concepts of metaphysical time and between magnitudes of different dimensions, as “specializations space (see Casasanto and Boroditsky, 2008). for time, space and quantity develop from a single magnitude sys- The processing of sensory information according to its spatial, tem operating from birth” (2003:484). ATOM does not describe temporal, and numerical properties is a requirement of the cen- the nature of a shared accumulation system as the mode-control tral nervous system. Navon (1978) “considered the issue of how model does. ATOM grounds the ontogeny of multi-dimension we apprehend stimuli that vary along several dimensions. We may magnitude estimation abilities on the basis of the need for action, often overlook some aspects, and sometimes be unable to ignore and the translation from sensory to motor, and this is germane others” (1978:3). He suggested that time occupies the dominant to infant development (i.e., Piaget’s sensorimotor stage from 0 to dimension, followed by space. In non-humans and humans, there 2 years). It is reasoned in ATOM that the infant is born with a are a variety of interaction effects between our estimates of time, “one-bit” magnitude system, and number sense is mapped onto space, and number, and these have been taken as support for the magnitude system, which is argued to have a spatial basis mode-control models of (sensory) time and number perception (given its emphasis for action). Frontiers in Integrative Neuroscience www.frontiersin.org March 2012 | Volume 6 | Article 7 | 1 Allman et al. Neuroscience of time and number The primary focus of our review is how we develop the abil- 2008; Buhusi and Meck, 2009a,b; Lustig, 2011)aswellasthe ity to integrate (or “stitch together”) representations of duration impressive ability of humans and other animals to learn and and numerosity magnitudes, operating at the level of processing adapt to the temporal and numerical qualities of environmental incoming sensory input, couched within the influential “mode- events (Skinner, 1938; Gibbon, 1977; Gibbon et al., 1997). The control” approach (Meck and Church, 1983). This assumes the mode-control model (for time and number) is related to “scalar substrate for time and number judgments can be represented by expectancy theory” (SET; for time only, Gibbon et al., 1984). an “accumulated” magnitude, and there is quantitative equiva- These types of accounts were stimulated by studies of rodents lence between an estimate of number and a unit of time (Meck (and pigeons) operating on fixed-interval schedules (an event et al., 1985)—space (area) will also be discussed but to a lesser occurs at a fixed period in time). With training, rats and pigeons extent (but see Gallistel, 1989). Accordingly, we refer to “time” demonstrate “expectancy” (or anticipation) of an event around (time sense) as the ability to estimate duration magnitude in the thetimeitisscheduled(Church and Gibbon, 1982; Roberts and seconds to minutes range, and “number” (number sense) as the Boisvert, 1998), and the accuracy of their temporal expectancies ability to estimate non-symbolic numerosity (i.e., number of dots (duration judgment) can be neuropsychologically manipulated in an array). (e.g., by pharmacological agents, task load, sensory qualities; e.g., There are three main areas of coverage in this review: see Meck, 1983, 1996). Their behavioral expectancies conform to the scalar property (discussed in the next section). Animals also 1. We discuss animal findings relating to the neuroscience of appear to perform “superstitious behaviors” (Skinner, 1948)or time and number sense (NEUTIN), and comparable human sequences of actions to “count” (or parse) the passage of time studies of time, space, and number magnitude estimation (Killeen and Fetterman, 1988). Rats, pigeons, and monkeys can in infants and adults. We also highlight cross-dimensional also discriminate the number of entities in a set when non- interaction effects (e.g., between time, space, and number) in numerical dimensions (such as surface area, density, perimeter, non-humans and humans. duration, and rate) are strictly controlled for, and their per- 2. We review the “mini-evolution” of the development of time formance reflects the use of similar analog representations of and number sense in infancy and childhood. We also com- number to those of adult humans (e.g., Fetterman and MacEwen, ment on the correspondence between number sense and 1989; Brannon and Terrace, 1998, 2000; Emmerton, 1998). These more advanced numerical abilities (symbolic representations animals can also be trained to press a lever a specific number of of number, counting, math ability), and how children are times (fixed-ratio schedules), and appear sensitive to the rate of considered to develop higher-order concepts of time, speed, reinforcement (rate is defined as number divided by time)—there distance and space. is also evidence that certain animals can perform simple arith- 3. Children with developmental disabilities, particularly those metic reasoning (addition, subtraction; see Gallistel and Gelman, with difficulties as they relate to time and number abilities 2000 for a fuller discussion). (developmental
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