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 or surround suppression are present at the onset of visual experience or require visual experience for their emergence. We characterized the development of these properties and their dependence on visual experience in ferrets. Visual experience was varied across three conditions: typical rearing, dark rearing, and dark rearing with daily exposure to simple sinusoidal gratings (14-16 hours 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.Significance StatementThe 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 if response properties that depend on interactions among multiple stimuli develop without experience. We find that the properties of crossorientation 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.

Targeted cortical stimulation reveals principles of cortical contextual interactions

“…Visual cortical neurons exhibit sublinear responses to the simultaneous presentation of two grating stimuli (Adelson and Movshon, 1982; Morrone et al, 1982; Morrone et al, 1987; DeAngelis et al, 1992; Heeger, 1992; Carandini et al, 1997; Simoncelli and Heeger, 1998; Reynolds and Heeger, 2009; Popovic et al, 2018), Because some of this suppression is likely present in the inputs to the cortex that arise from LGN (Freeman et al, 2002; Li et al, 2006; Priebe and Ferster, 2006), we designed an experiment to directly provide input to different regions of the cortical circuit itself, in order to separate cortical contributions to normalization from those of its inputs.…”

“…Our results are consistent with a study that performed sparse stimulation of nearby orientation columns in tree shrew (Huang et al, 2014). One might have expected to find species differences between tree shrew and ferret because the tree shrew primarily exhibits length-summation in layer 2/3 (Chisum et al, 2003) while ferret exhibits both length-summation and surround suppression (Rubin et al, 2015; Popovic et al, 2018), but both species showed non-specific spread of activity in layer 2/3.…”

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 naïve visual cortical neurons exhibit lower firing rates than experienced animals (Clemens et al, 2012;Popovic 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 2 age groups: visually naïve ("naïve": age P30-34, n = 10 animals, 23 cells) and visually experienced ("experienced": age P40-60, n = 11 animals, 29 cells).…”

“…Visual stimuli: 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;Popovic 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).…”