Time and Number: The Privileged Status of Small Values in the Brain

When dancing, one follows the rhythm without much conscious control, while also singing, entertaining a conversation, planning intricate sequences of steps, or estimating the time until the end of the song. Processing of rapid beats, in the sub-second range seems to be done automatically and doesn’t appear to interfere with timekeeping in the range of seconds or minutes, required for planning the steps, or estimating the duration left until the end of the song. This may be because the processing of rapid beats and slow sequences is split between different timing mechanisms and/ or the left and the right hemispheres of our brain (Hancock, 2011). Relatively distinct brain circuits process time in the millisecond, seconds-to-minutes, or circadian range (Buhusi and Meck, 2005), but the distinction blurs around 1-s intervals. Circadian timing, which operates over roughly 24 h, and controls functions such as the sleep–wake cycle and the metabolic processes, is based on a molecular clock in the suprachiasmatic nucleus (Gallego and Virshup, 2007; Allman and Meck, 2011). Millisecond timing engages a variety of specialized local circuits in the cerebellum (De Zeeuw et al., 2011), for fast and fine movement control, or in the auditory cortex, for speech processing (Nourski and Brugge, 2011). Finally, planning and motor control in the seconds range engages the cortico-striatal circuits, motor, parietal, and prefrontal cortices, both in animals (Meck et al., 2008; Buhusi and Meck, 2009) and humans (Coull et al., 2004, 2011; Stevens et al., 2007). The relative separation of these circuits explains why one can deal with different attributes simultaneously, but also raises the possibility of conflicts or cooperation between these circuits for time intervals around 1 s. The question of whether suband supra-second timing engages distinct brain circuits was recently investigated in patients with unilateral hemispheric lesions (Gooch et al., 2011). Rather than selecting patients by lesion, the study used voxelbased lesion-symptom mapping (Bates et al., 2003) in patients with various lesions, and evaluated the contribution of each voxel for the overall performance in all patients, thus tapping into the circuits critical for timing without using a priori assumptions regarding the location of interest. Three findings bear noting. First, patients with lesions in the frontal or parietal cortices were less accurate than controls, thus supporting neurobiological models of timing suggesting that cortico-striatal circuits (Matell and Meck, 2004; Buhusi and Meck, 2005; Oprisan and Buhusi, 2011) and parietal circuits (Leon and Shadlen, 2003) develop neural representations of time. Second, the right hemisphere was involved in timing both suband suprasecond timing, consistent with previous studies implicating right cortical regions in interval timing (Schubotz et al., 2000; Rubia et al., 2003; Smith et al., 2003; Coull et al., 2004; Meck and Malapani, 2004; Lewis and Miall, 2006; Bueti et al., 2008), and supporting the hypothesis that right dorsolateral prefrontal cortex is crucial for timekeeping (Lewis and Miall, 2006; Meck et al., 2008). Instead, the left temporal lobe was involved in timing sub-second durations only, consistent with its implication in processing fast, auditory information. Thus, whereas all durations required the same circuitry in the right hemisphere, only the shortest intervals (<1 s) involved additional left-hemisphere structures, suggesting millisecond timing may have a special status in the brain. This distinction between short (sub-second) and longer intervals (supra-second) is not unique to time. Remarkable parallels exist between counting and timing, such that it has long been thought that counting may tap into similar cognitive and neural mechanisms as that of time (Meck and Church, 1983; Walsh, 2003; Feigenson, 2007; Cantlon et al., 2009). Timing and counting abilities are found in a diverse range of non-human animal species, from honeybees and rats to dolphins and monkeys (Meck and Church, 1983; Cantlon and Brannon, 2007; Cordes et al., 2007; Dacke and Srinivasan, 2008), and they share striking similarities, including Weber’s law: The ease with which two durations or numbers are discriminated is based upon their ratio, not their absolute difference (Meck and Church, 1983; Cantlon and Brannon, 2007). All species share a system for representing time and number that must have arisen early in evolutionary history and is present early in development (Xu and Spelke, 2000; vanMarle and Wynn, 2006; Brannon et al., 2007, 2008 – see Gallistel, 1990). In fact, time and number may even be represented using a common metric, in which the representation of one count is equivalent to 200 ms of time (Meck and Church, 1983; but see Balci and Gallistel, 2006). Support for the claim that representations of time and number are derived from the same mechanism is also provided by neurobiological studies of numerical processing, which like those of temporal processing, implicate parietal areas and, at least early in development, this activation is unique to the right hemisphere (Rivera et al., 2005; Cantlon et al., 2006) as in the case of time. Furthermore, whereas both behavioral and neural evidence suggests a distinction between sub-second and suprasecond timing, a similar distinction exists between representations of small (<4 or 5) sets and larger sets. Behavioral data from adults, infants, non-human primates, and even mosquitofish reveal that small sets are treated differently than large sets (e.g., Trick and Pylyshyn, 1994; Hauser and Carey, 2003; Agrillo et al., 2008; Cordes and Brannon, 2009a,b). For example, when asked to rapidly identify the number of items in a set, adults reveal little to 2