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. 2012 Dec 12;32(50):18177-85.
doi: 10.1523/JNEUROSCI.3399-12.2012.

The Laminar Development of Direction Selectivity in Ferret Visual Cortex

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Free PMC article

The Laminar Development of Direction Selectivity in Ferret Visual Cortex

Jared M Clemens et al. J Neurosci. .
Free PMC article

Abstract

Sensory experience plays a critical role in the development of cortical circuits. At the time of eye opening, visual cortical neurons in the ferret exhibit orientation selectivity, but lack direction selectivity, which is a feature of mature cortical neurons in this species. Direction selectivity emerges in the days and weeks following eye opening via a process that requires visual experience. However, the circuit mechanisms that underlie the development of direction selectivity remain unclear. Here, we used microelectrodes to examine the laminar chronology of the development of direction selectivity around the time of eye opening to identify the locations within the cortical circuit that are altered during this process. We found that neurons in layers 4 and 2/3 exhibited weak direction selectivity just before natural eye opening. Layer 4 neurons in animals that had opened their eyes but were younger than postnatal day 35 (PND 35) exhibited modestly increased direction selectivity, but layer 2/3 cells remained as weakly tuned as before eye opening. Animals that had opened their eyes and were PND 35 or older exhibited increased direction selectivity in both layers 4 and 2/3. On average, initial increases in direction selectivity in animals younger than PND 35 were explained by increases in responses to the preferred direction, while subsequent increases in direction selectivity in animals PND 35 or older were explained by decreases in responses to the null direction. These results suggest that all cortical layers are influenced by sensory stimulation during early stages of experience-dependent development.

Figures

Figure 1.
Figure 1.
Direction selectivity and orientation selectivity increase in the days following eye opening. a, Tuning curves of example cells from layers 2/3 and 4 of V1 from each of the 3 groups. The degree of direction and orientation selectivity is expressed in terms of 1 − circular variance in direction space or orientation space, respectively (see Materials and Methods). b, Cumulative percentage of direction and orientation selectivity values across all layers for each age group. * indicates that all differences among groups are significant (Kruskal–Wallis test).
Figure 2.
Figure 2.
Changes in average spike tuning curves as a function of development. a–c, Average tuning curves across all N orientation-selective recording sites for each of the 3 age groups. All curves have been rotated such that the preferred direction corresponds to rightward motion. * indicates differences across conditions that were significant with p < 0.05 (Kruskal–Wallis test, with Kruskal–Wallis post hoc test). a, b, Neurons recorded from animals that had opened their eyes but were less than PND 35 exhibited increased spiking responses to the preferred direction compared with animals whose eyes were closed. b, c, Neurons recorded from animals that had opened their eyes and were PND 35 or older exhibited significantly decreased responses to the null direction and orthogonal orientation compared with younger animals.
Figure 3.
Figure 3.
Laminar development of direction selectivity around eye opening. a, Direction selectivity of single units recorded from each age group. Each black dot represents a single recording site. The y-axis indicates the normalized depth of the recording and the x-axis indicates the degree of direction selectivity, expressed as 1 − circular variance in direction space. The gray line running the length of each subfigure is the sliding median of 1 − DirCirVar, descending cortical depth. The vertical black line demarcates substantial direction selectivity, with dots falling to the right of the line exhibiting substantial direction selectivity. The horizontal dashed lines indicate the borders between layers 2/3 and 4 and 4 and 5/6. b, Cumulative percentage of direction selectivity in each age group as a function of layer. c, Cumulative percentage of direction selectivity of each layer as a function of age group. Again, the vertical line demarcates substantial direction selectivity. Layer 4 neurons exhibited progressive increases in direction selectivity at each stage, whereas layer 2/3 neurons only exhibited a significant increase in direction selectivity in animals that had opened their eyes and were PND 35 or greater.
Figure 4.
Figure 4.
Laminar development of orientation selectivity around eye opening. Identical format to Figure 3 but in reference to orientation selectivity. a, Orientation selectivity of single units recorded from each age group. Each black dot represents a single recording site. The y-axis indicates the normalized depth of the recording and the x-axis indicates the degree of orientation selectivity, expressed as 1 − circular variance. The gray line is the sliding median of 1 − CirVar, descending cortical depth. The vertical black line demarcates substantial orientation selectivity, with dots falling to the right of the line exhibiting substantial orientation selectivity. Horizontal dashed lines indicate the borders between layers 2/3 and 4 and 4 and 5/6. b, Cumulative percentage of orientation selectivity in each age group as a function of layer. c, Cumulative percentage of orientation selectivity of each layer as a function of age group. Vertical line demarcates substantial orientation selectivity. Neurons in layers 4 and 2/3 exhibited progressively increasing orientation selectivity across the examined groups.
Figure 5.
Figure 5.
Visual stimulation provided during the experiment did not substantially alter direction selectivity values. a, Relationship between the cortical depth of each cell versus the total duration of visual stimulation that had been provided to the animal at the time the cell was recorded. Note that this total duration of stimulation corresponds to the total time of stimulation in 8 or 12 directions plus a blank stimulus, and includes interstimulus intervals (63% of total stimulation time). b, Weak relationships between 1 − DirCirVar index values and total stimulation. Lines are linear fits, with the correlation coefficient shown. In an ANOVA, animal group (p < 0.001) and cortical layer (p < 0.001) explained a significant amount of the variation in 1 − DirCirVar, but total stimulation time did not (p = 0.48), suggesting that the stimulation provided during the experiment did not alter direction selectivity values.

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