Anatomy and Physiology of Macaque Visual Cortical Areas V1, V2, and V5/MT: Bases for Biologically Realistic Models

Abstract

The cerebral cortex of primates encompasses multiple anatomically and physiologically distinct areas processing visual information. Areas V1, V2, and V5/MT are conserved across mammals and are central for visual behavior. To facilitate the generation of biologically accurate computational models of primate early visual processing, here we provide an overview of over 350 published studies of these three areas in the genus Macaca, whose visual system provides the closest model for human vision. The literature reports 14 anatomical connection types from the lateral geniculate nucleus of the thalamus to V1 having distinct layers of origin or termination, and 194 connection types between V1, V2, and V5, forming multiple parallel and interacting visual processing streams. Moreover, within V1, there are reports of 286 and 120 types of intrinsic excitatory and inhibitory connections, respectively. Physiologically, tuning of neuronal responses to 11 types of visual stimulus parameters has been consistently reported. Overall, the optimal spatial frequency (SF) of constituent neurons decreases with cortical hierarchy. Moreover, V5 neurons are distinct from neurons in other areas for their higher direction selectivity, higher contrast sensitivity, higher temporal frequency tuning, and wider SF bandwidth. We also discuss currently unavailable data that could be useful for biologically accurate models.

Keywords: biomimetic; computational neuroscience; microcircuit; neural network; neuroinformatics.

Figure 1

Schematics of CO and ocular dominance modules in V1. The cylinders in L3 depict CO blobs and the lighter and darker columnar gray bands the ODCs, most emphasized in L4C (Hubel and Wiesel 1968). References for cortical thickness (range of means; Chow et al. 1950; Lund 1973; O’Kusky and Colonnier 1982b); layer thickness is drawn approximately to scale (Lund 1973); reported distance between CO blobs is the range across monkeys (Horton 1984; Landisman and Ts’o 2002); reported width of ODC is the range across monkeys (LeVay et al. 1975; Horton and Hocking 1996).

Figure 2

Connections between LGN, V1, V2, and V5 and within V1 and V2. For references, see Supplementary Table 1D. Top, middle, and bottom rows indicate interareal, intra-areal excitatory, and intra-areal inhibitory connections, respectively. LEFT COLUMN: Connectograms (Krzywinski et al. 2009) showing connections between distinct layers. Each colored segment in the circular perimeter indicates a cortical layer, sublayer, or CO compartment. Line width and color intensity indicate the robustness of the connection. Unknown strengths are marked as medium; for V2 interlaminar connections (middle and bottom connectograms), the paucity and qualitative character of the available studies did not allow us to estimate connection strength. The origin (soma) of a projection neuron is marked as a line slightly displaced from the outer edge of the circle, while its termination (axon terminals) is marked as a line reaching the outer edge of the circle. “Top left”: Interareal connections and connections between LGN and areas V1, V2, and V5. Black lines indicate FF connections and green lines FB connections. V2 L4P = L4 pale stripe (no distinction between lateral/medial stripes), L4IM = L4 interstripe (or pale stripe) medial, L4T = L4 thick stripe, L4IL = L4 interstripe (or pale) lateral, L4N = L4 thin stripe. All interareal connections are excitatory. “Middle left”: Local excitatory connections. “Bottom left”: Local inhibitory connections; none of the studies reviewed here identified the CO compartments. RIGHT COLUMN: Matrix of the connections. No connection (white squares) indicates that the connection either does not exist or was not studied. Red squares indicate excitatory connections and blue squares inhibitory connections. Color intensity indicates the strength of the connection.

Figure 3

FF pathways and specialization of functional compartments in LGN, V1, V2, and V5. TOP: Main LGN to V1 pathways (Hendrickson et al. 1978; Blasdel and Lund 1983; Kaplan 2003; Casagrande et al. 2007). Arrow thickness indicates the relative contribution of Parvo and Magno geniculocortical afferents to the different V1 layers. BOTTOM: Main FF pathways between V1, V2, and V5 (Sincich and Horton 2002; Sincich et al. 2007, 2010; Federer et al. 2013). In both top and bottom schematics, additional sparse connections were omitted for clarity. The CO compartments of V1 and V2 contain multiple functional feature maps, and their constituent neurons show specific RF tuning properties, as indicated on the right. Numbers refer to the following references: 1, Tootell et al. (1988a); 2, Landisman and Ts’o (2002); 3, Xiao et al. (2007); 4, Lu and Roe (2008); 5, Edwards et al. (1995); 6, Silverman et al. (1989); 7, Tootell et al. (1988a); 8, Gur and Snodderly (2007); 9, Felleman et al. (2015); 10, Shipp and Zeki (2002a); 11, Shipp and Zeki (2002b); 12, DeYoe and Van Essen (1985); 13, Roe and Ts’o (1995); 14, Munk et al. (1995); 15, Gegenfurtner et al. (1996); 16, Vanduffel et al. (2002); 17, Ts’O et al. (2001); 18, Levitt et al. (1994a); 19, Tootell and Hamilton (1989); 20, Peterhans and von der Heydt (1993); 21, Chen et al. (2008); 22, Lu et al. (2010); 23, Tootell et al. (2004); 24, Xiao et al. (2003); 25, Wang et al. (2007); 26, Lu and Roe (2007); 27, Roe et al. (2005); 28, Heider et al. (2000); 29, Lagae et al. (1993); 30, Maunsell and Van Essen (1983c); 31, Perrone and Thiele (2001); 32, Albright (1984); 33, Dubner and Zeki (1971); 34, Maunsell and Van Essen (1983a); and 35, DeAngelis and Newsome (1999).

Figure 4

Extent of intra-areal horizontal connections in the tangential domain of areas V1, V2, and V5. Horizontal connections in V1 are most prominent in L2/3 and 5 but exist also in L4B/upper 4Cα and 6 (Amir et al. 1993; Angelucci et al. 2002b). In V2, horizontally spreading connections emerge from L2 and L3 and some from L5 and L6 (Levitt et al. 1994b). In V5, locally projecting neurons are predominantly found in L2 and L3 and, following deep layer injections, also in L6 (Ahmed et al. 2012). In the center of each cortical slab is a halo (black dot) of dense, unspecific local connectivity, surrounded by more specific patches of terminal clusters (gray dots). In V1, the OD pattern (modified from LeVay et al. 1975) and, in V2, the schematics of the CO bands are approximately at scale. In V5, the darker shading in layers 4–6 depicts heavier myelination. The horizontal connection extents are average maxima across studies from M. fascicularis and M. mulatta: V1, (Amir et al. 1993; Angelucci et al. 2002b); V2 (Amir et al. 1993); and V5 (Ahmed et al. 2012).

Figure 5

Onset latencies of spiking responses to visual stimulation. The proportions of cells are displayed as a function of latency. The number of distinct figures providing the source data, some in the same papers, are indicated on the right (N data sets), together with the total number of cells across the data sets. Bar darkness reflects the number of cells in each bin, normalized to largest number of cells in any of the bins across the three cortical areas. The black bar on the right contains outlier values above the reported cutoff at the tick mark value. The whisker plots indicate the 2.5, 25, 50, 75, and 97.5 percentiles of the data, calculated from the histograms in the original data. Data for V1 are from Maunsell and Gibson (1992) and Nowak et al. (1995), for V2 from Nowak et al. (1995), and for V5 from Raiguel et al. (1989).

Figure 6

ASF in V1. (A) ASF for an example V1 neuron. Solid line represents fit to the data (dots) using the DoG model. Dashed line indicates the mean spontaneous firing rate. Arrows indicate the center and surround diameters obtained using the DoG fit. Arrowheads indicate the center and surround diameters extracted from the empirically measured responses (without any fit). Data from Shushruth et al. (2009). (B) RF center diameter with respect to eccentricity. Solid line represents linear fit to the data (dots, N = 425). (C) RF surround diameter with respect to eccentricity. Solid line represents linear fit to the data (dots, N = 425). (B and C) data from Cavanaugh et al. (2002).

Figure 7

CV. Conventions are as in Figure 5. Data for V1 are from Ringach et al. (2002), Gur et al. (2005), and Goris et al. (2015) and for V2 from Goris et al. (2015).

Figure 8

Orientation BW. Conventions are as in Figure 5. Data for V1 are from Ringach et al. (2002) and Gur et al. (2005), for V2 from Levitt et al. (1994a), and for V5 from Albright (1984).

Figure 9

DSI. Conventions are as in Figure 5. Data for V1 are from De Valois et al. (1982b), Albright (1984), Movshon and Newsome (1996), and Wang and Movshon (2016), for V2 from Levitt et al. (1994a), and for V5 from Maunsell and Van Essen (1983c), Albright (1984), Movshon and Newsome (1996), and Wang and Movshon (2016).

Figure 10

SF peak. Conventions are as in Figure 5. Data for V1 are from De Valois et al. 1982a and Foster et al. (1985), for V2 from Levitt et al. (1994a), and for V5 from Yuan et al. (2014).

Figure 11

SF BW. Conventions are as in Figure 5. Data for V1 are from Foster et al. (1985) and Wang and Movshon (2016), for V2 from Foster et al. (1985) and Levitt et al. (1994a), and for V5 from Wang and Movshon (2016).

Figure 12

TF peak. Conventions are as in Figure 5. Data for V1 are from Foster et al. (1985) and Hawken et al. (1996), for V2 from Foster et al. (1985) and Levitt et al. (1994a), and for V5 from Yuan et al. (2014).

Figure 13

TF BW. Conventions are as in Figure 5. Data for V1 are from Foster et al. (1985) and for V2 from Foster et al. (1985) and Levitt et al. (1994a).

Figure 14

Semisaturation contrast and contrast exponent of the contrast response function. Conventions are as in Figure 5. Data for V1 are from Sclar et al. (1990), for V2 from Levitt et al. (1994a), and for V5 from Sclar et al. (1990).

Figure 15

Contrast response function. Based on the median parameters of the data reported in Figure 14.

Figure 16

Maximum firing rate. Stimuli were sinusoidal gratings at 120 cd/m² luminance and saturating contrast; the grating orientation, SF, motion direction, and speed were optimized for each cell. Conventions are as in Figure 5. Data for V1 and V5 are from Sclar et al. (1990).

Figure 17

Describing connections between two neuron groups in silico. (A) A simple point-like phenomenological neural model with fixed synaptic dynamics only needs to incorporate data on position and population size as well as data on the divergence and convergence of connections. (B) A more comprehensive, biophysically meaningful, multicompartmental model requires, in addition, data on the cellular morphology, distribution of synapses, and electrical types of neurons and synaptic dynamics.