Layer-specific input to distinct cell types in layer 6 of monkey primary visual cortex

Abstract

Layer 6 of monkey V1 contains a physiologically and anatomically diverse population of excitatory pyramidal neurons. Distinctive arborization patterns of axons and dendrites within the functionally specialized cortical layers define eight types of layer 6 pyramidal neurons and suggest unique information processing roles for each cell type. To address how input sources contribute to cellular function, we examined the laminar sources of functional excitatory input onto individual layer 6 pyramidal neurons using scanning laser photostimulation. We find that excitatory input sources correlate with cell type. Class I neurons with axonal arbors selectively targeting magnocellular (M) recipient layer 4Calpha receive input from M-dominated layer 4B, whereas class I neurons whose axonal arbors target parvocellular (P) recipient layer 4Cbeta receive input from P-dominated layer 2/3. Surprisingly, these neuronal types do not differ significantly in the inputs they receive directly from layers 4Calpha or 4Cbeta. Class II cells, which lack dense axonal arbors within layer 4C, receive excitatory input from layers targeted by their local axons. Specifically, type IIA cells project axons to and receive input from the deep but not superficial layers. Type IIB neurons project to and receive input from the deepest and most superficial, but not middle layers. Type IIC neurons arborize throughout the cortical layers and tend to receive inputs from all cortical layers. These observations have implications for the functional roles of different layer 6 cell types in visual information processing.

Fig. 1.

Eight anatomical types of layer 6 pyramidal neurons in monkey V1. Cell type is labeled beneath each reconstruction. Dendrites are black, and axons are gray. Axons extending below layer 6 indicate cell types that sometimes (dashed lines) or always (solid lines) project out of V1. Laminar borders are depicted by thehorizontal lines and labeled to the leftof each row. Class I neurons are in the top row, and class II neurons are in the bottom row. Most cells shown are from Wiser and Callaway (1996), their Fig. 12. Camera lucida drawings were modified to allow accurate depictions of laminar specificity in the context of idealized, width-invariant cortical layers.

Fig. 2.

Functional excitatory input maps for individual class I (A, B, C) and class II (D, E, F) neurons. The colors at each location indicate linearly interpolated sum of EPSC amplitudes (minus spontaneous EPSCs) collected at photostimulation sites for each cell. Colors are scaled according to the scale bars between the plots. Laminar borders are represented by (near) horizontal lines and labeled to the left of the plots. Mean ± SEM of EPSC amplitude sums (in picoamperes; spontaneous EPSCs were not subtracted out, but are shown at the bottom right of each plot) for each layer are shown to the right of each plot. Asterisks next to mean ± SEM values indicate layers providing statistically significant input based on sum of EPSC amplitudes (single asterisk) or EPSC amplitude only (double asterisks) compared with spontaneous EPSCs. Camera lucida drawings of axons (thin white lines) and dendrites (thick) are overlaid onto plots. Gray areas are present so that neuronal processes can be seen against the otherwise white background; no photostimulation occurred within these areas. A, A type Iα neuron (cell number B48c11) (Table 1) received significant input from layers 4B, 4Cα, and 4Cβ, 5, and 6, but not from layer 2/3.B, A type IC neuron (A48c1) (Table 1) received significant input from layers 2/3, 5, and 6. C, A type Iβ neuron (B48c2) (Table 1) received significant input from layers 2/3, 4Cα, and 4Cβ, 5 and 6, but not from layer 4B.D, A type IIA neuron (A48c12) (Table 1) received significant input from layers 4C, 5, and 6 but not from layers above 4C. E, A type IIB neuron (B45c7) (Table 1) received significant input from layer 2/3, but not from the middle layers.F, A type IIC neuron (A43c4) (Table 1) received significant input from layers 2/3, 4A, 4B, 4C, and 5. The axons of the type IIC neuron shown leave the plane of the slice at the layer 4Cβ/5 border. Scale bars, 100 μm (shown at the top, right corner of each plot).

Fig. 3.

Laminar input to class I neurons.A, Percentages of class I neurons of each type receiving significant increases in EPSC amplitude, number, or sum of amplitudes compared with spontaneous trials for each cortical layer. *A smaller percentage of type Iα and Im neurons received significant layer 2/3 input compared with the other class I types (p = 0.03; Fisher's Exact test). **A larger percentage of type Iα and Im neurons received significant layer 4B input than the other class I types (p = 0.01). B, Mean ± SEM of NEIs (see Materials and Methods) for each layer and for each cell type. ***Type Iα and Im neurons received significantly weaker layer 2/3 input than other class I neurons (p = 0.02; Rank Sum test; type Iβ and IβA vs type Iα and Im, p = 0.04; type IC vs type Iα and Im, p = 0.07). ****Type IC neurons received stronger layer 6 input than type Iβ and IβA neurons (p = 0.045). Gray bars represent type Iα and Im cells, black bars represent type IC cells, and open barsrepresent type Iβ and IβA neurons.

Fig. 4.

Laminar input to class II neurons.A, Percentage of class II neurons of each cell type receiving significant input from each layer. *A smaller percentage of type IIA neurons received significant layer 2/3 input than type IIB and IIC neurons (p = 0.045; Fisher's Exact test). **A smaller percentage type IIB neurons received significant layer 4Cα input than the other types (p = 0.02; IIA vs IIB, p = 0.04; IIC vs IIB,p = 0.04). B, Mean ± SEM of NEIs from each cortical layer for each cell type. ***Type IIC neurons received stronger layer 2/3 input than type IIA neurons (p = 0.046; Rank Sum test). ****Type IIB neurons received weaker layer 4C input than type IIA or IIC neurons (p = 0.01 for both comparisons). Gray bars represent type IIA neurons, black barsrepresent type IIB neurons, and open bars represent type IIC neurons. Conventions are the same as for Figure 3.