Connectivity of neuronal populations within and between areas of primate somatosensory cortex
- 204 Downloads
Functions of the cerebral cortex emerge via interactions of horizontally distributed neuronal populations within and across areas. However, the connectional underpinning of these interactions is not well understood. The present study explores the circuitry of column-size cortical domains within the hierarchically organized somatosensory cortical areas 3b and 1 using tract tracing and optical intrinsic signal imaging (OIS). The anatomical findings reveal that feedforward connections exhibit high topographic specificity, while intrinsic and feedback connections have a more widespread distribution. Both intrinsic and inter-areal connections are topographically oriented across the finger representations. Compared to area 3b, the low clustering of connections and small cortical magnification factor supports that the circuitry of area 1 scaffolds a sparse functional representation that integrates peripheral information from a large area that is fed back to area 3b. Fast information exchange between areas is ensured by thick axons forming a topographically organized, reciprocal pathway. Moreover, the highest density of projecting neurons and groups of axon arborization patches corresponds well with the size and locations of the functional population response reported by OIS. The findings establish connectional motifs at the mesoscopic level that underpin the functional organization of the cerebral cortex.
KeywordsHorizontal connections Cortical hierarchy Cortical magnification Optical intrinsic signal imaging Tract tracing
Supported by the Fogarty International Research Collaboration Award, U.S. National Institutes of Health; Grant numbers: NS059061 (to A.W.R. and L.N.), NS044375 and NS093998 (to A.W.R.) as well as the Hungarian Scientific Research Fund; Grant number: OTKA NN79366 (to L.N.).
Fogarty International Research Collaboration Award, NS059061 (to A.W.R. and L.N.), U.S. National Institutes of Health NS044375 and NS093998 (to A.W.R.). Hungarian Scientific Research Fund; Grant number: OTKA NN79366 (to L.N.)
Compliance with ethical standards
Conflict of interest
The authors declare that they have no conflict of interest.
Research involving human participants and/or animals
This article does not contain any studies with human participants performed by any of the authors.
All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. Animal care and surgeries were performed according to NIH (National Institute of Health) regulations and were in compliance with and approved by the Institutional Animal Care and Use Committee of Vanderbilt University.
- Ashaber M, Pálfi E, Friedman RM, Palmer C, Jákli B, Chen LM, Kántor O, Roe AW, Négyessy L (2014) Connectivity of somatosensory cortical area 1 forms an anatomical substrate for the emergence of multifinger receptive fields and complex feature selectivity in the squirrel monkey (Saimiri sciureus). J Comp Neurol 522:1769–1785CrossRefPubMedPubMedCentralGoogle Scholar
- Buzás P, Kovács K, Ferecskó AS, Budd JM, Eysel UT, Kisvárday ZF (2006) Model-based analysis of excitatory lateral connections in the visual cortex. J Comp Neurol 881:499–861Google Scholar
- Ester M, Kriegel H, Sander J, Xu X (1996) A density-based algorithm for discovering clusters in large spatial databases with noise. KDD-96 Proc 34:226–231Google Scholar
- Horvát S, Gămănuț R, Ercsey-Ravasz M, Magrou L, Gămănuț B, Van Essen DC, Burkhalter A, Knoblauch K, Toroczkai Z, Kennedy H (2016) Spatial embedding and wiring cost constrain the functional layout of the cortical network of rodents and primates. PLoS Biol 14:e1002512CrossRefPubMedPubMedCentralGoogle Scholar
- Iwamura Y, Tanaka M, Sakamoto M, Hikosaka O (1983a) Functional subdivisions representing different finger regions in area 3 of the first somatosensory cortex of the conscious monkey. Exp Brain Res 51:315–326Google Scholar
- Iwamura Y, Tanaka M, Sakamoto M, Hikosaka O (1983b) Converging patterns of finger representation and complex response properties of neurons in area 1 of the first somatosensory cortex of the conscious monkey. Exp Brain Res 51:327–337Google Scholar
- Markov NT, Misery P, Falchier A, Lamy C, Vezoli J, Quilodran R, Gariel MA, Giroud P, Ercsey-Ravasz M, Pilaz LJ, Huissoud C, Barone P, Dehay C, Toroczkai Z, Van Essen DC, Kennedy H, Knoblauch K (2011) Weight consistency specifies regularities of macaque cortical networks. Cereb Cortex 21:1254–1272CrossRefPubMedGoogle Scholar
- Négyessy L, Pálfi E, Ashaber M, Zalányi L, Palmer C, Kántor O, Friedman RM, Roe AW (2015) Complementary role of intra- and inter-areal cortical connections in somatosensory processing in primates. Society for Neuroscience, ChicagoGoogle Scholar
- Négyessy L, Pálfi E, Zalányi L, Ashaber M, Palmer C, Kántor O, Friedman RM, Roe AW (2016) Comparison of intrinsic and inter-areal cortical connectivity in the somatosensory cortex. IBRO Workshop. Budapest, HungaryGoogle Scholar
- Pálfi E, Zalányi L, Ashaber M, Palmer C, Friedman RM, Roe AW, Négyessy L (2016) Intrinsic and interareal connections in the primate somatosensory cortex. 10th FENS Forum of Neuroscience, Copenhagen, DenmarkGoogle Scholar