Pathways for motion analysis: Cortical connections of the medial superior temporal and fundus of the superior temporal visual areas in the macaque

“Twelve scans were acquired per subject.”

“The circuit that serves as the source of all three pathways seems to integrate information equally from central and peripheral visual fields 56 and to represent space largely, though not exclusively, in egocentric frames of reference (FIG.”

“It receives visual projections from various areas belonging to the ‘dorsal visual stream’ (among them areas MST and MT) that are involved in the analysis of optic flow and motion (Maunsell and Van Essen, 1983; Ungerleider and Desimone, 1986; Boussaoud et al., 1990).”

“More recently, somewhat weak projections have been described from distant areas in the ventral (temporal occipital area, temporal area) (Distler et al., 1993) and dorsal visual pathways [medial superior temporal (MST) and lateral intraparietal area (LIP)] ( Boussaoud et al., 1990; Felleman and Van Essen, 1991; Rocklan…”

“The pathways linking cortical areas have been partially elucidated by numerous anterograde and retrograde tracing experiments that have collectively revealed a number of important organizational principles (Zeki and Shipp 1988; Boussaoud et al. 1990; Felleman and Van Essen 1991; Young 1992; Goodhill et al. 1995; Barba…”

“On the basis of macaque data (Gattass et al., 1988; Boussaoud et al., 1990), one also might expect relatively large receptive fields in V4v, another human area near V3A.”

“These parietal areas receive input from the cortex of the caudal superior temporal sulcus (Seltzer and Pandya, 1978, 1984, 1991; Maunsell and Van Essen, 1983; Andersen et al., 1990; Boussaoud et al., 1990), where several areas involved in the perception of motion have been identified (Zeki, 1974; Van Essen et al.”

“Prior to a plan being formed, visual input travels to the IPL via the temporal lobe and a “third” visual stream (Boussaoud et al. 1990).”

“In the superior temporal sulcus, cells were found within several motion-sensitive areas, including the middle temporal area (MT), the medial superior temporal area (MST), the fundus of the superior temporal area (FST), and the superior temporal polysensory area (STP), as well as within anterior portions of the sulcus…”

“Many of these projections to FEF have been observed (Leichnetz, 1980; Barbas and Mesulam, 1981; Petrides and Pan-dya, 1984; Huerta et al., 1987; Barbas, 1988; Colby et al., 1988; Leichnetz and Goldberg, 1988; Leichnetz, 1989; Seltzer and Pandya, 1989; Andersen et al., 1990a; Boussaoud et al., 1990).”

“Extensive findings illustrate that certain areas near to the intraparietal sulcus form part of a sensory-motor hierarchy, sharing reciprocal projections with extrastriate visual cortex and the frontal eye fields (Maunsell and van Essen, 1983; Ungerleider and Desimone, 1986; Andersen et al., 1990; Boussaoud et al., 199…”

“Consistent with these neuronal properties, STP receives inputs from the posterior parietal cortex (Jones & Powell, 1970; Anderson, Asanuma, Essick, & Siegel, 1990; Morel & Bullier, 1990; Baizer, Ungerleider, & Desimone, 1990), which is associated with spatial analyses, and from areas MST and FST in the posterior porti…”

“The STP area derives its input from the MST area in the dorsal pathway and the anterior inferiortemporal area in the ventral pathway (Boussaoud et al. 1990; Felleman & Van Essen 1991).”

“It appears that V 1, MT, and MSTd are arranged in a motion processing hierarchy (e.g., Maunsell and Newsome, 1987; Andersen, 1989; Boussaoud et al., 1990), where the responses in MT, still relatively simple and local, are combined into the massively complex responses of MSTd.”

“Numerous tracer studies have extensively characterized the pathways linking cortical areas and have revealed many important principles of organization (Aflalo and Graziano, 2011; Barbas and Rempel-Clower, 1997; Boussaoud et al., 1990; Felleman and Van Essen, 1991; Jouve et al., 1998; Kaas and Collins, 2001; Rockland,…”

“Further detailed physiological and anatomical studies yielded an elaborate route map describing the functional organization of the visual system [16,17].”

“Area 45 has paralimbic connections with the insula and with areas TF and TL of the parahippocampal gyrus (Boussaoud et al., 1990; Cavada and GoldmanRakic, 1989; Cipolloni and Pandya, 1999; Gerbella et al., 2010; Lavenex et al., 2002; Lewis and Van Essen, 2000; Maioli et al., 1998; Martin-Elkins and…”

“For the temporal cortex, we adopted the nomenclatures of Saleem and Tanaka (1996) and Boussaoud et al. (1990), and for the lower bank of the STS (lSTS), we also adopted the subdivision of Seltzer and Pandya (1978).”

“The two pathways are not completely separate: outputs from areas MSTI and MSTd also pass through the fundus of the superior temporal sulcus (FST) to the posterior and anterior sections of the superior temporal polysensory area (STPp and STPa, Boussaoud, Ungerleider, & Desimone, 1990 ).”

“This expanse of cortex undoubtedly includes a number of different areas, some of which are likely to be homologous with macaque visual areas, such as MST and FST (Desimone and Ungerleider, 1986), parietal areas LIP and VIP (Colby et al., 1993, 1996) and possibly polysensory areas such as STPp (Bruce et al., 1981).”

“However, FST is interconnected with the posterior parietal cortex (Boussaoud et al., 1990; Kaas & Morel, 1993; Lewis & Van Essen, 2000a), which contains multimodal neurons (Duhamel et al.”

“…(within 400 mm) Nisslstained sections using published cytoarchitectonic criteria (Friedman et al., 1986; Amaral et al., 1987; Barbas and Pandya, 1989; Cavada and Goldman-Rakic, 1989; Seltzer and Pandya, 1989; Boussaoud et al., 1990; Baizer et al., 1991; Schall et al., 1995; Burton et al., 1995).”

“…from a greater number of regions than the number of regions to which it sends ascending projections; e.g., V1 receives top-down projections from IT while sending no direct bottom-up projections to IT (Barone, Batardiere, Knoblauch, & Kennedy, 2000; Boussaoud, Ungerleider, & Desimone, 1990 ).”

“FST has fewer direction-sensitive cells and receives input from V4, which MST lacks (Boussaoud et al. 1990).”

“…connected, in addition to ventral prefrontal (Petrides & Pandya, 1984; Cavada & Goldman-Rakic, 1989b; Rozzi et al., 2006) and inferotemporal cortex (Boussaoud et al., 1990; Webster et al., 1994; Borra et al., 2007), also to subcortical limbic structures (Kievit & Kuypers, 1975; Selemon &…”

“It has been demonstrated that V3a shares connections with areas in both the temporal and the parietal cortex (e.g., Tootell et al., 1997), which is also the case for STS (Boussaoud et al., 1990; Harries and Perrett, 1991).”

“1A (Komatsu and Wurtz, 1988; Boussaoud et al., 1990)).”

“…Maunsell and Van Essen, 1983; Weller et al., 1984; Kennedy and Bullier, 1985; Weller and Kaas, 1985; Barbas, 1986, 1995; Andersen et al., 1990; Boussaoud et al., 1990; Morel and Bullier, 1990; Baizer et al., 1991; Colby and Duhamel, 1991; Webster et al., 1991, 1994; Sousa et al., 1991;…”

“This model, based on the ssumption that the left hemisphere directs attention redominantly to the contralateral right side, whereas he right hemisphere directs attention to both hemipheres, has been confirmed in the course of previous unctional imaging experiments using various behavoral tasks (Corbetta et al., 1993,…”

“and inconsistent one, inasmuch it was not found in most of our cases and it was not reported previously in a study of the connections of MST (Boussaoud et al. 1990).”

“Area 7a receives input from the lateral intrparietal area (Andersen et al. 1990; Lewis and Van Essen 2000), the medial intraparietal area (Boussaoud et al. 1990; Lewis and Van Essen 2000; Bota 2001), and the ventral intraparietal area (Lewis and Van Essen 2000; reviewed in Maunsell 1995).”

“Ungerleider and Desimone 1986; Colby et al. 1988; Boussaoud et al. 1990; Webster et al. 1994), myeloarchitectonic criteria have been used to identify specific parietal areas, namely the lateral and ventral intraparietal areas (LIP and VIP, respectively), PO and PEc (Fig. 2C).”

“Within the fundus of the macaque IPS exists VIP (Colby et al. 1993), an area known to receive input from both MT (Blatt et al. 1990; Maunsell and van Essen 1983; Ungerleider and Mishkin 1979) and MSTd (Baizer et al. 1991; Boussaoud et al. 1990).”

“Neuronal signals that carry motion information pass from the primary visual cortex (V1) to MT, and then to adjacent motion-sensitive visual areas, including areas MST and FST (Maunsell and Van Essen, 1983; Ungerleider and Desimone, 1986; Krubitzer and Kaas, 1990; Boussaoud et al., 1990; Movshon and Newsome, 1996).”

“…but the argument is considerably strengthened by the observation that MT provides the major input to the middle superior temporal area (MST) (Maunsell and Van Essen 1983; Boussaoud et al 1990), where cells do seem to be well equipped for the analysis of optic flow (Duffy and Wurtz 1991, 1995).”

“…bank (LIP) (Selzer and Pandya 1980; Maunsell and Van Essen 1983; Ungerleider and Desimone 1986; Neal et al. 1988; Cavada and Goldman-Rakic 1989a; Boussaoud et al. 1990; Baizer et al. 1991), and both projections overlap in the fundus, where VIP is located (Maunsell and Van Essen 1983;…”

“The striate and extrastriate regions connect to the parietal cortex ( Boussaoud et al., 1990 ), which in turn is reciprocally connected to the motor and premotor regions (Cavada and Goldman-Rakic, 1989; Kurata, 1991).”

“Notice that although the more posterior regions (mSTS and TEO; data not shown) respond well to scrambled stimuli, responses were lower in TEda (and TEdp; data not shown).”

“Both response types were encoded by FEF neurons with both narrow- and broad-spike waveforms, presumably corresponding to inhibitory interneurons and excitatory pyramidal neurons, respectively, and with diverse visual, visuomotor, and motor properties, albeit with different frequencies.”

“This anatomical evidence in the living brain is consistent with functional data and post-mortem dissections in human 34–36 and macaque 30,31,37 .”

“In our study, the projection from area TEO to the dorsal part of L was present in all 4 cases with injections of WGA-HRP but in none of the 3 cases with injections of 3H-AA, which is probably a reflection of the greater sensitivity of WGA-HRP (see Boussaoud et al., 1990).”

“FST has fewer direction-sensitive cells and has an input from V4 which MST lacks (Boussaoud et al., 1990), suggesting that it may be as much involved in form as motion analysis.”

“Here it is V6 that contains a relatively diffuse laminar distribution of terminals, an intermediate pattern thought to distinguish a so-called 'lateral' connection , between areas of equal rank (Maunsell and Van Essen, 1983a; Andersen et al., 1990a; Boussaoud et al., 1990).”

“Both streams originate from the primary visual areas: the dorsal stream goes through extrastriate visual areas and reaches the associative parietal areas, whereas the ventral stream reaches the inferotemporal cortex (Mishkin et al., 1983; Boussaoud et al., 1990).”

“…of layer III are in a position to sample 'feedforward input' (Rockland and Pandya, 1979; Felleman and Van Essen, 1991), feedback projections (some of which terminate in layer III, e.g. Boussaoud et al., 1990) and callosal projections (Cusick et al., 1984; Kennedy et al., 1986; Beck and Kaas, 1994).”

“Like neurons in MSTd, V6 neurons are direction- and speedselective, both respond well to large stimuli (Eifuku and Wurtz 1998; Galletti et al. 1999), and both receive strong direct V1 input (Boussaoud et al. 1990; Sousa et al. 1991; Palmer and Rosa 2006).”

“…are organized in spatial or However, there are several more interconnected areas constisomatotopic maps, i.e., they are related to the external space tuting this dorsal stream (Andersen et al. 1990a; Boussaoud et al. 1990; Felleman and van Essen 1991; Goodale andor single muscles and extremities.”