Development of Cross-Orientation Suppression and Size Tuning and the Role of Experience

Abstract

Many sensory neural circuits exhibit response normalization, which occurs when the response of a neuron to a combination of multiple stimuli is less than the sum of the responses to the individual stimuli presented alone. In the visual cortex, normalization takes the forms of cross-orientation suppression and surround suppression. At the onset of visual experience, visual circuits are partially developed and exhibit some mature features such as orientation selectivity, but it is unknown whether cross-orientation suppression is present at the onset of visual experience or requires visual experience for its emergence. We characterized the development of normalization and its dependence on visual experience in female ferrets. Visual experience was varied across the following three conditions: typical rearing, dark rearing, and dark rearing with daily exposure to simple sinusoidal gratings (14-16 h total). Cross-orientation suppression and surround suppression were noted in the earliest observations, and did not vary considerably with experience. We also observed evidence of continued maturation of receptive field properties in the second month of visual experience: substantial length summation was observed only in the oldest animals (postnatal day 90); evoked firing rates were greatly increased in older animals; and direction selectivity required experience, but declined slightly in older animals. These results constrain the space of possible circuit implementations of these features. The development of the brain depends on both nature-factors that are independent of the experience of an individual animal-and nurture-factors that depend on experience. While orientation selectivity, one of the major response properties of neurons in visual cortex, is already present at the onset of visual experience, it is unknown whether response properties that depend on interactions among multiple stimuli develop without experience. We find that the properties of cross-orientation suppression and surround suppression are present at eye opening, and do not depend on visual experience. Our results are consistent with the idea that a majority of the basic properties of sensory neurons in primary visual cortex are derived independent of the experience of an individual animal.

Development of visual motion integration involves coordination of multiple cortical stages

“…The overall decrease in V1 plaid responses was very pronounced in our data set. Note, however, that a previous study ( Popović et al, 2018 ) investigating the development of V1 cross-orientation inhibition in ferrets (i.e., looking at responses to plaids with dOri = 90 deg) did not observe changes in plaid responses between P40 and adulthood, something that will need to be resolved with further experiments (see also Discussion).…”

“…Visual experience has been shown to play a key role in the development of direction selectivity in ferret V1 ( Li et al, 2006 ; Popović et al, 2018 ; Van Hooser et al, 2012 ). Here, we made use of inter-animal variability in development to begin to probe whether it might similarly impact the development of higher-level motion functions in ferrets.…”

Synaptic and intrinsic mechanisms underlying development of cortical direction selectivity

“…In order to examine the initial state of spatiotemporal receptive fields ( Figure 1 ) and to understand how these fields are altered during the short critical period for the emergence of direction selectivity, we carried out in vivo intracellular recordings in the visual cortex of anesthetized ferrets using sharp microelectrodes. Intracellular recordings were used because naive visual cortical neurons exhibit lower firing rates than experienced animals ( Clemens et al, 2012 ; Popović et al, 2018 ), and we wanted to be able to examine the receptive field properties of the subthreshold voltage in addition to spiking. Experimental animals were split in to two age groups: visually naive (‘naive’: age P30-34, n = 10 animals, 23 cells) and visually experienced (‘experienced’: age P40-60, n = 11 animals, 29 cells).…”

“…Visual stimuli were created in MATLAB with the Psychophysics Toolbox ( Brainard, 1997 ; Pelli, 1997 ; Kleiner et al, 2007 ) on a Macintosh Pro running OSX and displayed on a Dell monitor 1704FPVt (40 cm viewing distance). Gratings were shown in pseudorandom order at temporal frequencies that varied between 2–8 Hz and a spatial frequency of 0.08 cycles per degree, which is in the middle of the maximal response functions for animals in this age range ( Li et al, 2006 ; Popović et al, 2018 ). Sparse noise stimuli for reverse correlation analysis were 1-dimensional bar stimuli, rotated so that the bar orientation matched the preferred orientation of each cell ( Priebe and Ferster, 2005 ; Rust et al, 2005 ).…”

Postnatal Development of Visual Cortical Function in the Mammalian Brain

“…Direction selectivity in area 17 necessitates visual experience for even basic development in ferrets but not mice (Li et al, 2006;Rochefort et al, 2011). Cross-orientation suppression and surround suppression are present at eye opening in ferrets, thus suggesting that visual experience is not necessary for their emergence but is necessary for sustaining these functions (Popović et al, 2018). In preterm monkeys with light exposure, synapse formation proceeds normally, but for further fine tuning of RF properties visual experience is necessary (Bourgeois et al, 1989;Yuste et al, 1992;Anderson et al, 1993;Bourgeois and Rakic, 1996;Callaway, 1998;DeAngelis et al, 1999).…”