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Gateways of Ventral and Dorsal Streams in Mouse Visual Cortex Quanxin Wang Washington University School of Medicine in St

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Gateways of Ventral and Dorsal Streams in Mouse Visual Cortex Quanxin Wang Washington University School of Medicine in St Washington University School of Medicine Digital Commons@Becker Open Access Publications 2011 Gateways of ventral and dorsal streams in mouse visual cortex Quanxin Wang Washington University School of Medicine in St. Louis Enquan Gao Washington University School of Medicine in St. Louis Andreas Burkhalter Washington University School of Medicine in St. Louis Follow this and additional works at: https://digitalcommons.wustl.edu/open_access_pubs Part of the Medicine and Health Sciences Commons Recommended Citation Wang, Quanxin; Gao, Enquan; and Burkhalter, Andreas, ,"Gateways of ventral and dorsal streams in mouse visual cortex." The ourJ nal of Neuroscience.,. 1905-1918. (2011). https://digitalcommons.wustl.edu/open_access_pubs/226 This Open Access Publication is brought to you for free and open access by Digital Commons@Becker. It has been accepted for inclusion in Open Access Publications by an authorized administrator of Digital Commons@Becker. For more information, please contact [email protected]. The Journal of Neuroscience, February 2, 2011 • 31(5):1905–1918 • 1905 Behavioral/Systems/Cognitive Gateways of Ventral and Dorsal Streams in Mouse Visual Cortex Quanxin Wang, Enquan Gao, and Andreas Burkhalter Department of Anatomy and Neurobiology, Washington University School of Medicine, St. Louis, Missouri 63110 Itiswidelyheldthatthespatialprocessingfunctionsunderlyingrodentnavigationaresimilartothoseencodinghumanepisodicmemory (Doeller et al., 2010). Spatial and nonspatial information are provided by all senses including vision. It has been suggested that visual inputs are fed to the navigational network in cortex and hippocampus through dorsal and ventral intracortical streams (Whitlock et al., 2008), but this has not been shown directly in rodents. We have used cytoarchitectonic and chemoarchitectonic markers, topographic mapping of receptive fields, and pathway tracing to determine in mouse visual cortex whether the lateromedial field (LM) and the anterolateral field (AL), which are the principal targets of primary visual cortex (V1) (Wang and Burkhalter, 2007) specialized for processingnonspatialandspatialvisualinformation(Gaoetal.,2006),aredistinctareaswithdiverseconnections.Wehavefoundthatthe LM/AL border coincides with a change in type 2 muscarinic acetylcholine receptor expression in layer 4 and with the representation of the lower visual field periphery. Our quantitative analyses also show that LM strongly projects to temporal cortex as well as the lateral entorhinal cortex, which has weak spatial selectivity (Hargreaves et al., 2005). In contrast, AL has stronger connections with posterior parietal cortex, motor cortex, and the spatially selective medial entorhinal cortex (Haftig et al., 2005). These results support the notion that LM and AL are architecturally, topographically, and connectionally distinct areas of extrastriate visual cortex and that they are gateways for ventral and dorsal streams. Introduction Goodale, 2010). It has been proposed that circuits in the rodent Visual information is used for object recognition, moving eyes visual system are organized in similar fashion (Kolb, 1990; Mc- and head, reaching, grasping, and navigation (Whitlock et al., Donald and Mascagni, 1996). However, there is little detailed 2008). It is widely held that these functions rely on basic spatial understanding of the network that carries different forms of vi- processing mechanisms that are similar to those used for encod- sual information from V1 to temporal, posterior parietal, and ing episodic memory (Knierim et al., 2006; Bird and Burgess, motor cortex. 2008; Eichenbaum and Lipton, 2008; Doeller et al., 2010). The Classic studies have shown that mouse V1 sends output to two neuronal network that underlies these functions is known to in- regions in medial and seven regions in lateral extrastriate visual terconnect the visual cortex with somatosensory, posterior pari- cortex (Olavarria and Montero, 1989). In rats and mice, the etal, motor, temporal, and parahippocampal areas as well as the strongest inputs terminate on the lateral side of V1 at two sites hippocampus (Bird and Burgess, 2008; Whitlock et al., 2008). within an island that receives few callosal inputs (Coogan and Navigation relies on the perception of landmarks and the pro- Burkhalter, 1993; Wang and Burkhalter, 2007). Topographic cessing of path integration information about the speed and the mapping studies of connections from V1 and recordings of re- direction of self-motion (Whitlock et al., 2008). The task of the ceptive fields have shown that each of these regions contains visual system, then, is to deliver nonspatial information about complete representations of the contralateral visual field that be- landmarks and spatial information about their topographic rela- long to separate areas, the lateromedial field (LM) and anterolat- tionships including cues about self-location to the network. In eral field (AL) (Wang and Burkhalter, 2007). Both of these areas the primate visual system, this diverse information is carried by have also been identified by mapping of intrinsic optical signals interconnected streams that preferentially link areas in ventral (Schuett et al., 2002; Tohmi et al., 2009). Based on the distinctive and dorsal cerebral cortex (Ungerleider and Mishkin, 1982; connections and the shared vertical meridian representation with V1, it was suggested that LM corresponds to primate V2 (Coogan Received July 5, 2010; revised Nov. 17, 2010; accepted Dec. 3, 2010. and Burkhalter, 1993; Wang and Burkhalter, 2007). Although This work was supported by National Eye Institute Grant RO1EY016184, the McDonnell Center for System Neu- differences in neurofilament, serotonin, and cytochrome oxidase roscience, and the Human Frontier Science Program 2000B. We thank Justin Horowitz for developing Matlab soft- ware and Katia Valkova for excellent technical assistance. The content of this manuscript is solely the responsibility expression were found in lateral extrastriate cortex (Remple et al., of the authors and does not necessarily represent the official views of the National Eye Institute or the National 2003; Hamasaki et al., 2004; Van der Gucht et al., 2007), it re- Institutes of Health. mains unclear whether LM and AL are chemoarchitectonically Correspondence should be addressed to Andreas Burkhalter, Department of Anatomy and Neurobiology, Wash- distinct. Recordings indicate that LM and AL are functionally ington University School of Medicine, 660 South Euclid Avenue, St. Louis, MO 63110-1093. E-mail: burkhala@ pcg.wustl.edu. diverse (Gao et al., 2006), suggesting that high spatial resolution DOI:10.1523/JNEUROSCI.3488-10.2011 information flows through LM to temporal cortex, whereas in- Copyright © 2011 the authors 0270-6474/11/311905-14$15.00/0 formation about fast-moving objects flows through AL into the 1906 • J. Neurosci., February 2, 2011 • 31(5):1905–1918 Wang et al. • Ventral and Dorsal Streams in Mouse Visual Cortex posterior parietal cortex. Here, we exam- ined whether LM and AL are chemoarchi- tectonically and connectionally distinct. The results show an abrupt decrease in type 2 muscarinic acetylcholine receptor (m2AChR) expression at the LM/AL bor- der. In addition, distinctive pathways sug- gest that LM is a gateway to the ventral stream, whereas AL preferentially pro- vides inputs to the dorsal stream. Materials and Methods Experiments were performed in postnatal day 10 (P10) and 6- to 8-week-old C57BL/6J male and female mice. All experimental procedures were approved by the Institutional Animal Care and Use Committee at Washington Uni- versity and conformed to the National Insti- tutes of Health guidelines. Mapping chemoarchitecture of cortex For mapping the chemoarchitecture, we have used immunostaining of different markers to- gether with retrograde labeling of callosal con- nections in tangential sections of flatmounts of the left cerebral hemisphere. Sectioning the cor- tex in the tangential plane is critically important in animals with small brains in which the spatial resolution of graphically reconstructed labeling patterns from coronal sections limits the accu- racy of making maps of chemoarchitectonic re- gions (Paxinos and Franklin, 2001; Van der Figure 1. LM/AL border identified by the transition of m2AChR expression coincides with receptive field recordings from lower Gucht et al., 2007). In addition, labeling of cal- visual field. A, Expression of m2AChR in a tangential section through layer 4 in left adult visual cortex. The arrowheads mark the losal landmarks in the same sections is invaluable LM/AL border between the m2AChR-expressing area LM and the nonexpressing area AL. B, Density contour map of m2AChR for assigning chemoarchitectonic fields and con- expression showing a Ն20% reduction of immunostaining at the LM/AL border (arrowheads). C, D, Overlay of m2AChR with nections to specific cortical areas and regions FR-labeled callosal connections. Numbered rows in C indicate recording sites in areas LM and AL. The receptive fields at site 1 (Wang and Burkhalter, 2007). (posteriorgreenmark)areintheuppervisualfield(D),droptothelowervisualfield(site5,middlegreenmark)attheLM/ALborder Newborn P10 mice were anesthetized by in- (C, D, arrowheads), and reverse back to upper fields (site 8, anterior green mark) in AL (C, D). A second series of recordings (sites halation of 2.5% isofluorane (Butler) in oxy- 9–18) shows a similar trend with a reversal at site 15. Note that the recordings sites 5 and 15 coincide with the transition
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