Review articleStructure and function of the middle temporal visual area (MT) in the marmoset: Comparisons with the macaque monkey
Introduction
Over the last several decades, the various species of macaque monkey (genus Macaca) have been the dominant primate models in neuroscience, leading to the discovery of many important principles of visual physiology, cognition and pathology (e.g. Kuypers et al., 1965, Hubel and Wiesel, 1968, Wurtz, 1969, Zeki, 1969, Gross et al., 1972). However, marmoset monkeys (genus Callithrix) are rapidly emerging as an attractive alternative for studies of visual processing, given what is already a substantial body of anatomical and physiological studies of their visual pathways (Solomon and Rosa, 2014), as well as a number of key advantages, relative to the macaque, in the application of modern techniques for the study of brain function at the cellular and circuit levels. For example, the marmoset's smaller and lissencephalic cortex should allow more efficient and systematic study of extrastriate visual areas by new technologies such as “grid” (planar) multielectrode arrays (Warren et al., 2001, Torab et al., 2011) and multiphoton imaging (Ohki et al., 2005). In particular, the geometry of the marmoset brain will allow this type of study to be substantially expanded, to encompass the entire extent of a visual area, or multiple areas, concurrently. In addition, marmosets are easily bred in captivity, and mature quickly in comparison with macaques (Chandolia et al., 2006, Nishijima et al., 2012). These characteristics have proven advantageous in the context of developmental studies (e.g. Yu et al., 2013), as well for the creation of transgenic lines (e.g. Sasaki et al., 2009, Okano et al., 2012). Finally, marmosets have been used in experiments involving complex operating behaviours (e.g. Roberts et al., 1990, Maclean et al., 2001, Derrington et al., 2002, Barefoot et al., 2003, Clarke et al., 2004, Clarke et al., 2011, Spinelli et al., 2004, Yamazaki et al., 2011, Nakako et al., 2013), and it has recently been demonstrated that they can perform visual discrimination tasks involving the control of eye movement when the head is stabilized (Mitchell et al., 2014). Together with the development of techniques for functional MRI analysis of neural signals in awake marmosets (Belcher et al., 2013, Liu et al., 2013), this has significantly expanded the scope of experiments in these animals, particularly with respect to the contributions of visual areas to perception and behaviour.
To date, relatively few studies have examined the response properties of neurons in marmoset extrastriate visual cortex. Marmosets have to perform visual processing with a brain that is 12 times smaller (in mass) than that of macaques, and nearly 200 times smaller than the human brain (Stephan et al., 1981, Palmer and Rosa, 2006, Chaplin et al., 2013). An important question, which is amenable to comparative anatomical and physiological analyses, is what processing strategies allow brains with fewer neurons to code for the same amount of visual space. This can be answered by studying species of various sizes with highly frontalized eyes, including marmosets, macaques and humans. The insights from such analyses will provide information on the commonalities and differences between the brains of human and non-human primates.
In this review, we focus on comparing the middle temporal area (MT) in marmoset and macaque monkeys (Fig. 1). MT is an early processing area of the extrastriate cortex, which is considered to be shared by all primates (Rosa, 1999, Rosa, 2002). It is also the most intensively studied area of the extrastriate cortex, thus providing the best available basis for anatomical and functional comparisons across species. Although most of what we presently know about area MT derives from studies in the macaque, this area was in fact discovered independently in New and Old World monkeys (Allman and Kaas, 1971, Dubner and Zeki, 1971). Among the defining characteristics of area MT which are likely shared by all primates are its dense myelination (Allman and Kaas, 1971), the clear directional selectivity in the responses of most of its neurons (Dubner and Zeki, 1971, Maunsell and Van Essen, 1983, Albright, 1984, Felleman and Kaas, 1984, Solomon et al., 2011, Lui et al., 2012), and the fact that it receives its anatomical inputs directly from neurons located in layer IVb in the primary visual cortex (V1; Spatz, 1977, Ungerleider and Desimone, 1986a, Shipp and Zeki, 1989, Rosa et al., 1993). In macaques, single cell activity in MT has been causally linked to motion perception (Britten et al., 1996); moreover, altering the activity in its neurons via microstimulation leads to behavioural effects in motion perception (Salzman et al., 1992, Ditterich et al., 2003), and lesions of this area lead to deficits in motion discrimination (i.e., Newsome and Pare, 1988, Pasternak and Merigan, 1994). Thus, MT is usually regarded as the key component of the brain's motion analysis system.
Despite differences in overall brain size, the ratio between the surface area of MT and that of V1 is approximately the same across all primates (Krubitzer and Kaas, 1990, Pessoa et al., 1992, Rosa, 2002). Moreover, the ability to integrate synaptic inputs, estimated by measures such as the relative sizes of neuronal dendritic trees of pyramidal neurons, and their numbers of dendritic spines, is very similar in V1 and MT of marmosets and macaques (Elston et al., 1999). Therefore, the convergence of inputs from V1 to MT is likely to be conserved, at least to a first approximation. Moreover, MT forms a first order representation of the entire contralateral visual field, which can be regarded approximately as a scaled version of the V1 map (Allman and Kaas, 1971, Rosa and Elston, 1998). Indeed, it has been proposed that MT shares important characteristics with the primary sensory cortices, including early development and post-natal maturation (Rosa and Tweedale, 2005, Bourne and Rosa, 2006).
Section snippets
Direction selectivity and response rates
In marmosets, as in macaques, the overwhelming majority of MT neurons are strongly direction selective. Representative examples of cells showing this response property are illustrated in Fig. 2(A and B). This result is upheld whether the moving stimuli used in the tests are gratings (Lui et al., 2007a, Lui et al., 2007b), kinetic dot patches (Solomon et al., 2011), single luminance-defined objects, such as bars (Lui et al., 2012), or textured patterns (Lui et al., 2012, Gharaei et al., 2013).
Neuronal responses in animals with V1 lesions
In adult primates, most visual information first arrives at the level of the cortex at V1, which forms an anatomical “gateway” through which most visual information enters the extrastriate cortex. As V1 is retinotopic, human patients (and monkeys) who suffer damage to V1 lose conscious vision in “islands” of the visual field (scotomas), which correspond to the representation of the damaged area (Horton and Hoyt, 1991, Moore et al., 2001, Kato et al., 2011). Interestingly, it was found that
Anatomical connections of marmoset MT
It has been suggested that patterns of neuronal connections change systematically as a function of overall brain size, and that such changes are likely to have functional consequences (e.g. Rilling and Insel, 1999, Changizi and Shimojo, 2005, Striedter, 2005). For example, modelling studies have proposed that the patterns of cortical connections will likely vary, with larger brains requiring more segregation between subsystems of areas in comparison with smaller brains in order to maintain a
Possible functional implications of findings in area MT for visual processing in marmosets
It is clear now that visual acuity is lower in marmosets, in comparison with macaques. Indeed, our finding of lack of responses to higher spatial frequencies in marmoset MT reflects a likely more general feature of visual processing in this species, including the retina (Wilder et al., 1996), and other stages of early visual processing (for review, see Solomon and Rosa, 2014). Individual objects comprise multiple spatial frequencies; in fact, lower spatial frequencies tend to dominate natural
Concluding remarks
In this review, we have focused on MT, which is considered to be a “core” visual area of the primate cortex. We have highlighted the many similarities, but also a few differences between the marmoset and the macaque, two of the species for which substantial knowledge about this area has been obtained. One rich subject for future work will be to determine the perceptual and cognitive consequences of the rearrangements of neural resources, associated with overall changes in brain size, taking
Acknowledgements
Both LL and MR are funded by the Australian Research Council (ARC) Special Initiative in Bionic Vision and Technology (SR1000006; Monash Vision Group) and ARC Centre of Excellence for Integrative Brain Function (CE140100007). LL is funded by an early career award from the ARC (DECRA 130100493) and also by the National Health and Medical Research Council of Australia (NHMRC; Project Grants 1003906, 1066232). MR also receives funding from the NHMRC (Project grants: 1028710 and 1020839). We thank
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