Receptive-field properties of V1 and V2 neurons in mice and macaque monkeys

Abstract

We report the results of extracellular single-unit recording experiments where we quantitatively analyzed the receptive-field (RF) properties of neurons in V1 and an adjacent extrastriate visual area (V2L) of anesthetized mice with emphasis on the RF center-surround organization. We compared the results with the RF center-surround organization of V1 and V2 neurons in macaque monkeys. If species differences in spatial scale are taken into consideration, mouse V1 and V2L neurons had remarkably fine stimulus selectivity, and the majority of response properties in V2L were not different from those in V1. The RF center-surround organization of mouse V1 neurons was qualitatively similar to that for macaque monkeys (i.e., the RF center is surrounded by extended suppressive regions). However, unlike in monkey V2, a significant proportion of cortical neurons, largely complex cells in V2L, did not exhibit quantifiable RF surround suppression. Simple cells had smaller RF centers than complex cells, and the prevalence and strength of surround suppression were greater in simple cells than in complex cells. These findings, particularly on the RF center-surround organization of visual cortical neurons, give new insights into the principles governing cortical circuits in the mouse visual cortex and should provide further impetus for the use of mice in studies on the genetic and molecular basis of RF development and synaptic plasticity.

Figure 1

Reconstruction of electrode tracks and recording sites in V1 (A) and V2L (B) in mouse visual cortex. Adjacent sections where the electrode track and lesions were not visible are shown in C and D. Layers are easily identifiable and indicated on the left and right. Electrolytic lesions at the end of penetrations are labeled. Preferred orientation of each unit is also indicated by a short bar. Note that in V1 (A), there were two penetrations and the second penetration that was made perpendicular to the surface ended in layer 4. The penetration in panel B shows that the majority of units were from V2L except the first 3 units that were in V1. WM signifies the white matter. The markers indicate the location of the borders between V1 and V2L and V2L and auditory cortex. V1 could be distinguished from V2L by its thicker layer 4 and a less densely packed layer 5, in particular immediately above layer 6 where a sublayer with fewer cells is visible in V1 but not V2L.

Figure 2

(A) Frequency distributions of F₁/F₀ ratios for mouse cell population (n=96). Cells with the ratio ≥ 1.0 were classified as simple cells and those having the ratio < 1.0 were classified as complex cells (Skottun et al., 1991). The frequency distribution for V1 cells is indicated by open bars (n=69), for V2L cells by filled bars (n=27). (B) Layer differences in F₁/F₀ ratio in mouse V1 (open circles) and V2L (closed squares). Circles or squares indicate the median values while short bars indicate quartile values. The number at the top indicates the number of units for each group.

Figure 3

Representative tuning curves for stimulus orientation (A-B), spatial frequency (C-D), temporal frequency (E-F), and contrast (G-H) in mice.

Figure 4

Frequency distributions of spatial and temporal response properties and contrast sensitivity of V1 and V2L neurons in mice. Histograms of orientation/direction selectivity (A-C), spatial frequency selectivity (D-F), temporal frequency selectivity (G-I), and contrast sensitivity (J-L). In each panel, open bars indicate V1 neurons and filled bars represent V2L neurons with corresponding triangles indicating median values.

Figure 5

Relationships between response attenuation at low spatial frequency (LSFV) and spatial frequency bandwidth (A) and circular variance (CV) (B) in mice. V1 neurons are shown in black triangles, V2L units by red circles.

Figure 6

Frequency distributions of spatial and temporal response properties and contrast sensitivity of simple and complex cells of V1 and V2L neurons in mice. Histograms of orientation/direction selectivity (A-C), spatial frequency selectivity (D-F), temporal frequency selectivity (G-I), and contrast sensitivity (J-L). In each panel, open bars indicate simple cells and filled bars represent complex cells with corresponding triangles indicating median values.

Figure 7

Layer differences in orientation (A-C) and spatial frequency tuning (D-F) and spontaneous (G) and peak (H) firing rates in mice. Circles indicate the median values and short bars indicate quartile values. The sample size for each layer group is the same as that in Fig 2B.

Figure 8

Relationships between the spontaneous activity and the peak firing rate, spatial and temporal tuning properties and contrast sensitivity of mouse V1 and V2L neurons. Frequency distribution of spontaneous activity of V1 (open bars) and V2L (Filled bars) neurons (A), and peak firing rate (B). Peak firing rate as a function of spontaneous activity in V1 (open circle) and V2L (open square) (C). Spatial and temporal tuning properties and contrast sensitivity (D-O) as a function of spontaneous firing rates. Cells were arbitrarily divided into low (sp < 1.0 spikes/sec), middle (1.0 < sp < 10.0 spikes/sec, and high (sp > 10/spikes/sec) spontaneous groups.

Figure 9

Representative size tuning functions of V1 (A-D) and V2 neurons (E-H) in mice (top: A,B,E,F) and macaque monkeys (bottom: C,D,G,H). Data points were fitted with the ratios of Gaussians (Cavanaugh et al., 2002). For each species, units with and without surround suppression are illustrated.

Figure 10

Receptive field center and surround properties of V1 and V2 neurons in mice and monkeys. Frequency distribution of V1 (open bars) and V2 (filled bars) neurons of RF center size (A), surround size (B), suppression index (C) and surround/center size ratio (D) in mouse visual cortex. Triangles indicate median values. Frequency distributions of center size (E), surround size (F), suppression index (G) and surround/center size ratio (H) in monkeys. No Srd signifies those neurons without measurable RF surrounds.

Figure 11

Receptive field center and surround properties of V1 and V2 neurons in mice and monkeys. Frequency distribution of simple cells (open bars) and complex cells (filled bars) of RF center size (A), surround size (B), suppression index (C) and surround/center size ratio (D) in mouse visual cortex. Triangles indicate median values. Frequency distributions of center size (E), surround size (F), suppression index (G) and surround/center size ratio (H) in monkeys. No Srd signifies those neurons without measurable RF surrounds.

Figure 12

Correlation between the strength of RF surround suppression (SI) and RF center size (A), surround size (B), and surround/center size ratio (C) of individual neurons in mice (red) and monkeys (black). Triangles signify V1 neurons and circles indicate V2 neurons. Dotted lines with r-values indicate fit for mice and continuous lines with r-values indicate fit for monkeys.

Figure 13

Layer differences in center size (A, E), surround size (B, F), suppression index (C, G) and surround/center size ratio (D, H) in mice (A-D) and monkey (E-H). Circles and squares indicate the median values of V1 and V2L units respectively and short bars indicate quartile values. Numbers of units per layer and brain region are indicated on top.