- Email: [email protected]
Lateral masking effects on contrast sensitivity in rats
Accepted Manuscript Title: Lateral Masking Effects on Contrast Sensitivity in Rats Authors: Daniel D. Kurylo, Sowmya Yeturo, Joseph Lanza, Farhan Bukhari PII: DOI: Reference:
S0166-4328(17)30573-9 http://dx.doi.org/doi:10.1016/j.bbr.2017.07.046 BBR 11018
To appear in:
Behavioural Brain Research
Received date: Revised date: Accepted date:
2-4-2017 11-7-2017 29-7-2017
Please cite this article as: Kurylo Daniel D, Yeturo Sowmya, Lanza Joseph, Bukhari Farhan.Lateral Masking Effects on Contrast Sensitivity in Rats.Behavioural Brain Research http://dx.doi.org/10.1016/j.bbr.2017.07.046 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
Lateral masking effects in rats 8/5/2017
Lateral Masking Effects on Contrast Sensitivity in Rats Daniel D. Kurylo1, Sowmya Yeturo1, Joseph Lanza1, and Farhan Bukhari2 1 Department
of Psychology, Brooklyn College CUNY, Brooklyn, NY 11210
2 Department
of Computer Science, The Graduate Center CUNY, New York, NY 10016
Corresponding author: Daniel D. Kurylo Psychology Department Brooklyn College CUNY 2900 Bedford Avenue Brooklyn, NY 11210
Phone: 718-951-5000 x 6022 Fax: 718-951-4814 e-mail: [email protected]
Highlights
Visual contrast sensitivity in rats is reduced by adjacent, non-overlapping masks
Lateral mask effects were unaffected by relative orientation or separation of masks
Results are consistent with non-systematic orientation topography in rodent cortex
Abstract Changes in target visibility may be produced by additional stimulus elements at adjacent locations.
Such contextual effects may reflect lateral interactions of stimulus
representations in early cortical areas. It has been reported that the organization of orientation preference found in primates and cats visual cortex differs from that found in rodents, suggesting functional distinctions across species. In order to examine effects of
1
Lateral masking effects in rats lateral interactions at a perceptual level, contrast sensitivity in rats was measured for Gabor patches masked by two additional patches. Rats responded to target onset, and perceptual indices were based upon reaction time distributions across levels of luminance contrast.
It was found that contrast sensitivity of targets without lateral masks
corresponded to levels previously reported. For all measurements, the presence of sustained lateral masks systematically reduced sensitivity to targets, demonstrating interference by adjacent elements across levels of contrast. Effects of mask orientation or separation were not observed. These results may reflect reported non-systematic topography of orientation tuning across the cortex in rodents. Results suggest that intrinsic lateral connections in early processing areas play a minimal role in stimulus integration for rats.
keywords: animal perception; animal psychophysics; visual cortex; cortical integration; lateral flankers
1. Introduction
Visibility of stimulus components may be enhanced or diminished by the presence of adjacent stimulus elements. Such effects are evident with high-contrast lateral masks [1], metacontrast with zero stimulus onset asynchrony [2], and crowding of peripheral targets [3]. Contextual effects on perceptual capacities may reflect neural interactions among representations of targets and lateral masks. At a neural level, response properties of cortical neurons are modulated by the context in which stimuli are placed [4,5,6]. In primates and cats, systematic relationships exist among the orientation preference of neurons. Such connections may contribute to a system of enhancement and inhibition of signals based upon contextual effects from other cortical sites [7,8]. In rodents, the distribution of orientation preference is not systematic [9,10], nor do lateral projections display the periodic patches found in primates and cats [11]. These distinctions in cortical organization suggest that lateral interactions among stimulus elements may operate differently in rats than in primates and cats.
2
Lateral masking effects in rats At a perceptual level, the ability of rats to discriminate the presence or absence of targets declined when target onset was accompanied by flankers [12]. In addition, misses as well as false alarms increased when flankers were collinear to targets, compared to flankers that deviated from collinearity. Such effects on detecting suprathreshold stimuli were observed across a range of contrasts of both targets and flankers [13]. For humans, contrast thresholds are elevated in the presence of collinear, co-axial Gabor patches positioned near test stimuli (within 2 cycles), whereas thresholds decrease with adjacent elements positions within a farther zone (approximately 3 – 10 cycles) [14]. Flanker effects appear to be restricted to near foveal viewing [15,16] to which attention is directed [17,16], and are not observed at suprathreshold levels [15]. Flanker effects may reflect a system for contour integration mediated by short- and long-range interactions within neural populations [18]. The functional significance of connection patterns in local cortical circuits may be distinguished across species [19]. In order to explore lateral masking on detection thresholds in rats, responses to target onset were measured across luminance contrast for targets presented alone, or in the presence of masks.
2. Methods
2.1. Subjects Ten Long-Evans hooded rats served as subjects, each randomly assigned to one or more stimulus conditions. Animals were deprived of water for 22 hours before each session, and allowed water ad lib for one hour following sessions. Sessions occurred five days each week, and animals were allowed water ad lib on the remaining two days. This study was conducted in accordance with the National Institutes of Health Guide for the Care and Use of Laboratory Animals, and approved by the Institutional Animal Care and Use Committee of Brooklyn College. 2.2. Apparatus Behavioral measurements were made in a customized operant conditioning chamber (Figure 1A). The front panel of the chamber supported a metal funnel that extended 3 cm outside of the chamber. Animals had access to the funnel through a 5 cm diameter
3
Lateral masking effects in rats hole, centered 2.5 cm from the chamber floor. Placement of the rat's head completely within the funnel disrupted an infrared (IR) light beam connecting an emitter/detector pair mounted at the tip of the funnel. Rats viewed the stimulus through holes in the funnel positioned over each eye. Viewing stimuli from the head-fitted funnel allowed control over viewing position across trials. Rats had access to an enclosed drinking well positioned next to the funnel. A measured amount of water was delivered to the drinking well by means of a solenoid driven valve. Circuitry for the IR pair and solenoid were interfaced via solid-state relay switches to a computer. Stimulus generation, data collection, and trial events were controlled in real-time by customized computer software [20].
2.3. Stimulus Presentation In an otherwise darkened room, stimuli were presented on a computer monitor (Trinitron CPD 4401) controlled by a graphics adaptor (NVidia GeForce FX5200) set to 1280 x 1024 pixel resolution. Rats viewed stimuli at a distance of 24 cm and elevated by 10°, centered within the binocular region of the visual field. Stimuli consisted of Gabor patches on a gray background (22.3 cd/m2). Luminance levels were linearized across a range of 2.9 to 42.2 cd/m2.
2.4. General Procedure Using a free-operant procedure, rats initiated trials by placing their head into a central funnel. Following a delay, generated randomly between 500 and 2000 ms, a Gabor patch appeared on the monitor. Rats were trained to remain stationary until stimulus onset, to which they responded by withdrawing their head from the funnel (Figure 1B). Following training, data collection occurred on approximately every other session. In order to maintain consistence performance, a session of maintenance training occurred on alternate days.
2.5. Training Procedure
4
Lateral masking effects in rats Following initial magazine training, rats were trained to nose-poke the central funnel. The next phase of training required rats to remain stationary in the funnel for increasing lengths of time, culminating with a 500 ms hold period. A high-contrast Gabor patch was presented on the monitor at the end of the required hold period. For the next phase of training, stimulus onset varied randomly between 500 - 750 ms, and rats were required to withdraw their head from the funnel within 750 ms of stimulus onset. Across training sessions, stimulus onset times progressively increased to 500 - 2000 ms, and reaction time to stimulus onset was progressively restricted to 50 - 400 ms. Progressive increase to stimulus onset range, and progressive decrease in reaction time window, was contingent upon rats' performance, requiring 90% correct across a single session. For data collection sessions, reward was delivered on each trail, regardless of reaction time. In order to maintain conditioning, each session of data collection was followed by a training session.
2.6. Reaction Time Cluster Index Reaction time was recorded from stimulus onset to head withdrawal. Frequency distributions of reaction times, time-locked to stimulus onset, were displayed as histograms. High-contrast stimuli produced reaction time distributions that clustered about a mean of 237 ms (S.D. 104 ms). Given the unpredictable onset time of stimuli, the clustering pattern of reaction time distributions verified behavioral control by the stimulus. Quantification of reaction time clustering was based upon the incidence of responses that occurred above that found on no-stimulus trials. Specifically, the distribution of response frequency (histogram bin height) across reaction time was first determined for no-stimulus trials (Figure 2A). The upper boundary of the nominal distribution was set to 2 S.D. above the distribution mean. Reaction time distributions were then measured for each stimulus condition (Figure 2B). For each contrast level, the sum of response frequencies above the nominal boundary served as the response index.
5
Lateral masking effects in rats 2.7. Psychophysical Measurements Detection thresholds were determined with the psychophysical Method of Constant Stimuli. For each condition, reaction time distributions were compiled for each of six contrasts, as well as a no-stimulus condition, presented in random order across trials. No-stimulus trials were therefore randomly interleaved among the stimulus-present trials. For each contrast level, reaction time distributions were based upon approximately 150 trials, collected across multiple sessions. For no-stimulus trials, reaction times were calculated from a randomized presentation time (between 500 - 2000 ms from trial initiation), thereby corresponding to conditions for the stimulus-present trials. Examples of reaction time frequency distributions across contrast are depicted in Figure 3. For high-contrast stimuli, response frequency above the nominal boundary was approximately 25%, and progressively declined with reduced contrast. Response indices, plotted across contrast, are described well by a sigmoidal function. Threshold contrast, extrapolated from the sigmoidal function, was set to a response index of 2.5%. This value corresponds to the initial elevation in the psychometric function.
2.8. Stimulus Conditions Contrast thresholds were measured for targets alone, or in the presence of masks that varied in orientation and lateral separation.
2.8.1. Contrast Sensitivity. Contrast sensitivity was determined for 0.21 cpd, which corresponds to near peak sensitivity for Long-Evans rats [21,23], and 0.40 cpd, which corresponds to approximately the midpoint of the high-frequency limb of the CSF. The 0.21 cpd patch subtended a visual angle of 14.0°, in which approximately 2.5 cycles were visible.
The 0.40 cpd patch was presented at two sizes, 14.0° and 5.9°, in which
approximately 5.5 and 2.5 cycles were visible, respectively.
2.8.2. Lateral Mask. For the lateral mask condition, masks, set to a Michelson contrast of 0.53, were positioned above and below test stimuli. In all cases, lateral masks
6
Lateral masking effects in rats matched test stimuli spatial frequency and size. For the 0.21 cpd condition, lateral masks were positioned 2.8 cycles from test stimuli centers. For the 0.40 cpd condition, lateral masks were positioned 5.7 (for patch size 14.0°) and 2.8 cycles (for patch size 5.9°) from test stimuli. Lateral masks existed before rats placed their head into the funnel, and remained visible throughout the trial. Rats thereby responded to the onset of test stimuli, without additional cues introduced by mask onset.
2.8.3. Lateral Mask Orientation.
To investigate effects of relative orientation,
performance was compared between lateral masks that were collinear or orthogonal to test stimuli. Orientation effects were examined for 0.21 and 0.40 cpd, with a patch size of 14.0°.
2.8.4. Lateral Mask Separation. To investigate effects of lateral mask separation, performance was compared across lateral masks positioned 2.8, 4.8, and 6.8 cycles from test-stimulus centers. Separation effects were examined for the 0.21 cpd, 5.9° size condition. In all cases, lateral masks were collinear to test stimuli.
3. Results
For high-contrast stimuli, response indices reached approximately 25%, although some rats did not reach this level even with the maximum contrast. In order to equate variation in behavioral patterns across rats, response indices were normalized to 25%. For each condition, response indices as a function of contrast were determined separately for each rat. Best-fit sigmoidal functions were then determined for each rat, from which 2.5% thresholds were extrapolated. Statistical analyses were then applied to response thresholds.
3.1. Contrast Sensitivity. Mean response indices are depicted for each condition (Figure 4). A sigmoidal function fit to response indices is also shown in order to demonstrate the response
7
Lateral masking effects in rats pattern.
Mean contrast threshold at 0.21 cpd was 7% (Michelson), and contrast
thresholds at 0.40 cpd were 13% and 18% for the large and small targets, respectively. For large targets, contrast thresholds differed significantly between 0.21 and 0.40 cpd (Mann-Whitney U = 0, p < .05). Contrast thresholds for the two target sizes at 0.40 cpd also differed significantly (U = 0, p < .05). Examining performance across contrast, responses at 0.21 and 0.40 cpd differed significantly (p < .05). A trend existed across intermediate contrasts for the size factor at 0.40 cpd, although differences reached significance only for 22% contrast.
3.2. Lateral Mask Effects. Mean response indices across contrast, with best-fit functions, are displayed in Figure 5. Performance with masks was reduced compared to targets alone for intermediate levels of contrast. Specifically, for the 0.21 cpd condition, performance with masks differed significantly from target alone for contrasts between 16 - 28% (U = 1.5 at each contrast; p < 0.05). For 0.40, 14.0° condition, masks vs. target alone conditions differed significantly for contrasts between 16 - 36% (across contrasts U ranged from 1.00 to 2.5 ; p < 0.05). For the 0.40 cpd, 5.9° condition, masks and target alone conditions differed significantly for contrasts between 16 - 22% (U ranged from 1.00 to 2.00; p < 0.05). Comparing contrast sensitivity, lateral masks reduced sensitivity for each of the stimulus conditions (Figure 6). Sensitivity with masks was significantly lower than with target alone for the 0.21 cpd (U = 4.00; p < 0.05), 0.40 cpd, 14.0° (U = 5.50; p < 0.05), and 0.40 cpd, 5.9° (U = 5.50; p < 0.05) conditions.
3.3. Orientation Effects Performance was similar for collinear and orthogonal masks for both the 0.21 (Figure 7B) and 0.40 cpd conditions (Figure 7D). Comparing performance at each level of
8
Lateral masking effects in rats contrast, collinear and orthogonal mask conditions did not differ significantly for either the 0.21 or 0.44 cpd conditions (Mann-Whitney, p > 0.05).
3.4. Separation Effects Performance was similar for mask separations of 5.2, 8.4, and 11.8 cpd (Figure 7F). Comparing results at each level of contrast, performance did not differ significantly across levels of mask separation (Kruskal-Wallis, p > 0.05).
4. Discussion
These results demonstrate a masking effect in rats on contrast sensitivity by stimuli positioned at adjacent, non-overlapping positions. In this regard, lateral interactions of stimulus components are apparent at a perceptual level. As with suprathreshold stimuli [12,13], contrast thresholds in rats are elevated in the presence of lateral masking. Contrast sensitivities reported here for target alone are similar to previous studies, although sensitivity measurements reported here are greater than those from previous reports [21,22,23]. Differences may reflect distinctions in stimulus parameters, including wave pattern, target size, and mean luminance, as well as psychophysical techniques. In addition, head position was regulated in the current study in order to preclude introducing additional visual cues. Free moving rats may introduce visual cues produced by lateral head movements that reduce the ability to specify parameters such as luminance or spatial frequency [24]. Similarly, specifying stimulus metrics, including luminance and spatial frequency, requires regulation of stimulus position relative to the corneal surface [25,26,27]. Nevertheless, limitations in psychophysical measures in rats may obscure perceptual effects, such that sensitivity differences across masking conditions may be less than measurement resolution. In addition, because flanker effects on contrast thresholds are restricted to regions near the fovea [15,16], eye position, which is not controlled in rat measurements, may affect sensitivity. This issue may be further complicated by retinal characteristics of rats, in which area centralis and farther eccentric regions encode stimuli at a lower sampling density than occurs with primate foveal fixation [28,29].
9
Lateral masking effects in rats Performance did not differ significantly between relative orientation or among levels of separation. These results differ from those of Meier et al. [12], where flanker orientation affected target detection. Whereas some aspects of stimulus presentation were similar to those used here, significant procedural differences may account for differences in results. Procedures employed by Meier et al. allowed measures of response choice across levels of stimulus configurations. Rats made a two-alternative forced-choice response indicating "yes" or "no" to the presence of the target. Increased missed targets and increased false alarm rates occurred when targets and flankers were collinear, compared to misalignment conditions. In contrast, target detection measured here was based upon the reaction time distribution relative to the onset of the target. Across trials, flankers were either not presented, or had been visible before trials were initiated. Procedural differences between the studies may affect response factors, including perceptual decision. Although procedures used here allow high sensitivity to target detection, they may not allow sufficient measurement resolution to distinguish performance across differences in relative orientation of targets and flankers.
4.1. Mechanisms of integration. Differences in perceptual capacities across species may be associated with neural circuitry in early visual areas. In primates and cats, V1 topography displays a systematic pattern of orientation preference [30,31,32]. In addition, relative neural responses are enhanced by stimuli in adjacent areas that match a cell's orientation preference, and suppressed by stimuli that deviate from the preferred orientation [4,33,34,35]. In rats, a proportion of cells in primary visual cortex are selective for orientation [36,37,38,9]. Horizontal neural connections, found mainly in layers 2/3 and 5, project laterally within the same layer [39,40,41] as well as crossing layers [42]. Horizontal connections in rats extend laterally to 2 mm [40,41], linking neurons with overlapping receptive fields [39]. However, rodents display a heterogeneity of orientation preference in early cortical areas [9,10]. The absence of orientation effects reported here may reflect the locally disordered topography of orientation preference. As such, characteristics of local cortical connections in rats may be reflected at a perceptual level. Integration of stimulus elements in rats may be less associated with intrinsic lateral connections in early cortical areas, and more with long-range interactions, such as convergence across visual areas. Cortical mediation of pattern perception in rats is associated with both striate and lateral prestriate cortex [43,44,45]. Cortical areas in rats receive retinal input from two pathways, one passing from dorsal lateral geniculate
10
Lateral masking effects in rats nucleus to striate cortex, the other passing from superior colliculus to lateral posterior nucleus of the thalamus, and on to medial and lateral prestriate cortex and higher cortical areas [24,46,47]. The alternate pathway includes connections that bypass primary cortex, providing input to high-order areas not dependent on subordinate processing in striate cortex. Higher levels of processing that contain larger receptive fields perform more global analyses of stimuli, and are therefore well suited for integrating forms. Rats are capable of object recognition with transformation of stimulus characteristics, such as size, rotation, or position [48,49]. Systematic analysis of stimulus components indicates that recognition in rats is based upon integrating a pattern of object features, as opposed to a specific low-level stimulus characteristic [25]. In rats, lesions to areas 35 and 36, which show functional similarities to primate inferotemporal cortex [50], disrupt discrimination involving the conjunctions of features, suggesting that these regions contain configural representations of stimuli [51]. Pattern regularities among stimulus elements may thereby be processed at later stages, in which global relationships among stimulus components are encoded. Acknowledgements This work was supported by the City University of New York PSC-CUNY Research Award Program.
11
Lateral masking effects in rats References [1] Polat, U., and Sagi, D. (1994). The architecture of perceptual spatial interactions. Vision Research, 34, 73-78. [2] Breitmeyer, B., and Ganz, L. (1976). Implications of sustained and transient channels for theories of visual pattern masking, saccadic suppression, and information processing. Psychological Review, 83, 1-36. [3] Grainger, J., Tydgat, I., and Issele, J. (2010). Crowding affects letters and symbols differently.
Journal of Experimental Psychology, Human Perception and
Performance, 36, 673-688. [4] Angelucci, A., Levitt, J.D., Walton, E.J., Hupe, J.M., Bullier, J., and Lund, J.S. (2002b). Circuits for local and global integration in primary visual cortex.
Journal of
Neuroscience, 22, 8633-8646. [5] Bringuier, V., Chavane, F., Glaeser, L., and Fregnac, Y. (1999).
Horizontal
propagation of visual activity in the synaptic integration field of area 17 neurons. Science, 283, 695-699. [6] Kapadia, M.K., Ito, M., Gilbert, C.D. and Westheimer, G. (1995). Improvement in visual sensitivity by changes in local context: parallel studies in human observers and in V1 of alert monkeys. Neuron, 15, 843-856. [7] Alonso, J.M. (2002). Neural connections and receptive field properties in the primary visual cortex. Neuroscientist, 8, 443-456. [8] Angelucci, A., Levitt, J.D., Lund, J.S. (2002a). Anatomical origins of the classical receptive field and modulatory surround field of single neurons in macaque visual cortical area V1. Progress in Brain Research 136, 373-388. [9] Ohki, K., Chung, S., Ch'ng, Y.H., Kara, P., and Reid, R.C. (2005). Functional imaging with cellular resolution reveals precise microarchitecture in visual cortex. Nature, 433, 597-603. [10] Van Hooser, S.D., Heimel, J.A., Chung, S., Nelson, S.B., and Toth, L.J. (2005). Orientation selectivity without orientation maps in visual cortex of a highly visual mammal. Journal of Neuroscience, 25, 19-28.
12
Lateral masking effects in rats [11] Van Hooser, S.D., Heimel, J.A., Chung, S., and Nelson, S.B. (2006). Lack of patchy horizontal connectivity in primary visual cortex of a mammal without orientation maps. Journal of Neuroscience, 26, 7680 – 7692. [12] Meier, P., Flister, E., and Reinagel, P. (2011). Collinear features impair visual detection by rats. Journal of Vision, 11, 119-122. [13] Meier, P., and Reinagel, P. (2013). Rats and humans differ in processing collinear visual features. Frontiers in Neural Circuits, 7, 1-8. [14] Polat, U., and Sagi, D. (1993). Lateral interactions between spatial channels: suppression and facilitation revealed by lateral masking experiments.
Vision
Research, 33, 993-999. [15] Williams, C.B., and Hess, R.F. (1998). Relationship between facilitation at threshold and suprathreshold contour integration. Journal of the Optical Society of America, 15, 2046-2051. [16] Shani, R., and Sagi, D. (2005). Eccentricity effects on lateral interactions. Vision Research, 45, 2009-2024. [17] Freeman, E., Sagi, D., and Driver, J. (2001). Lateral interactions between targets and flankers in low-level vision depend on attention to the flankers.
Nature
Neuroscience, 4, 1032-1036. [18] Andini, Y., Sagi, D., and Tsodyks, M. (1997). Excitatory-inhibitory networks in the visual cortex: psychophysical evidence. Proceedings from the National Academy of Science, 94, 10426-10431. [19] Kaschube, M. (2014). Neural maps versus salt-and-pepper organization in visual cortex. Current Opinion in Neurobiology, 24, 95-102. [20] Bukhari, F., and Kurylo, D.D. (2008). Computer programming for generating visual stimuli. Behavior Research Methods, 40, 38-45. [21] Birch, D. & Jacobs, G.H. (1979). Spatial contrast sensitivity in albino and pigmented rats. Vision Research, 19, 933-937. [22] Legg, C.R., and Turkish, S. (1983).
Spatial contrast sensitivity changes after
subcortical visual system lesions in the rat. Behavioural Brain Research, 7, 253-259. [23] Legg, C.R. (1984). Contrast sensitivity at low spatial frequencies in the hooded rat. Vision Research, 24, 159-161.
13
Lateral masking effects in rats [24] Dean, P. (1990). Sensory Cortex: Visual Perceptual Functions. In B Kolb RC Tees (eds), The Cerebral Cortex of the Rat. Cambridge, MA: MIT Press, pp. 275-307. [25] Alemi-Neissi, A., Rosselli, F.B., and Zoccolan, D. (2013).
Multifeatural shape
processing in rats engaged in invariant visual object recognition.
Journal of
Neuroscience, 33, 5939-5956. [26] Kurylo, D.D. (2008). Effects of visual cortex lesions on perceptual grouping in rats. Behavioural Brain Research, 190, 182-188. [27] Kurylo, D.D., Van Nest, J., and Knepper, B. (1997). Characteristics of perceptual grouping in rats. Journal of Comparative Psychology, 111, 126-134. [28] Cowey, A., Franzini, C. (1979). The retinal origin of uncrossed optic nerve fibers in rats and their role in visual discrimination. Experimental Brain Research, 35, 443– 455. [29] Cowey, A., and Perry, V.H. (1979). The projection of the temporal retina in rats, studied by retrograde transport of horseradish peroxidase.
Experimental Brain
Research, 35, 457-464. [30] Blasdel, G.G., and Salama, G. (1986). Voltage-sensitive dyes reveal a modular organization in monkey striate cortex. Nature, 321, 579-585. [31] Grinvald, A., Lieke, E., Frostig, R.D., Gilbert, C.D., and Wiesel, T.N. (1986). Functional architecture of cortex revealed by optical imaging of intrinsic signals. Nature, 324, 361-364. [32] Polimeni. J.R., Granquist-Fraser D., Wood R.J., and Schwartz E.L. (2005). Physical limits to spatial resolution of optical recording: clarifying the spatial structure of cortical hypercolumns. Proceedings of the National Academy of Science, U S A, 102, 41584163. [33] Bosking, W.H., Zhang, Y., Schofield, B., and Fitzpatrick, D. (1997). Orientation selectivity and the arrangement of horizontal connections in tree shrew striate cortex. Journal of Neuroscience, 17, 2112-2127. [34] Crook, J.M., Engelmann, R., and Löwel, S. (2002). GABA-inactivation attenuates collinear facilitation in cat primary visual cortex. Experimental Brain Research, 143, 295-302.
14
Lateral masking effects in rats [35] Kasamatsu, T., Polat, U., Pettet, M.W., Norcia, A.M. (2001). Colinear facilitation promotes reliability of single-cell responses in cat striate cortex. Experimental Brain Research, 138, 163-172. [36] Parnavelas, J.G., Burne, R.A., and Lin, C.S. (1981). Receptive field properties of neurons in the visual cortex of the rat. Neuroscience Letters, 27, 291-296. [37] Girman, S.V., Sauve, Y., and Lund, R.D. (1999). Receptive field properties of single neurons in rat primary visual cortex. Journal of Neurophysiology, 82, 301-311. [38] Wiesenfeld, Z., and Kornel, E.E. (1975). Receptive fields of single cells in the visual cortex of the hooded rat. Brain Research, 94, 401-412. [39] Rumberger, A., Tyler, C.J., Lund., J.S. (2001). Intra- and inter-areal connections between the primary visual cortex V1 and the area immediately surrounding V1 in the rat. Neuroscience, 102, 35 - 52. [40] Burkhalter, A, and Charles, V. (1990). Organization of local axon collaterals of efferent projections neurons in rat visual cortex. Journal of Comparative Neurology, 302, 920 - 934. [41] Telfeian, A.E., and Connors, B.W. (2003). Widely integrative properties of layer 5 pyramidal cells support a role for processing of extralaminar synaptic input in rat neocortex. Neuroscience Letters, 343, 121-124. [42] Ichinose T Murakoshi T (1996). Electrophysiological elucidation of pathways of intrinsic horizontal connections in the rat visual cortex. Neurosci, 73, 25 - 37. [43] McDaniel, W.F., Coleman, J., and Lindsay Jr, J.F. (1982). A comparison of lateral peristriate and striate neocortical ablations in the rat. Behavioural Brain Research, 6, 249-272. [44] McDaniel, W.T., and Nobel, L.M. (1984). Visual pattern discrimination following bilateral striate or lateral peristriate neocortical injuries. IRCS Journal of Medical Science, 12, 1084-1085. [45] Lindsay, J.F., and McDaniel, W.F. (1987). Neural tissue transplants in rats with lateral peristriate lesions: II Behavior. Med Sci Res, 15, 655-656. [46] Sefton, A.J., and Dreher, B. (1985). Visual System In G Paxinos (ed), The Rat Nervous System, Vol 1 Forebrain and Midbrain. Sydney: Academic Press, , pp. 169221.
15
Lateral masking effects in rats [47] Zarrinpar, A., and Callaway, E.M. (2006). Local connections to specific types of layer 6 neurons in the rat visual cortex. Journal of Neurophysiology, 95, 1751-1761. [48] Tafazoli, S., Di Filippo, A., and Zoccolan, D. (2012). Transformation-tolerant object recognition in rats revealed by visual priming. Journal of Neuroscience, 32, 21-34. [49] Zoccolan, D., Oertelt, N., DiCarlo, J.J., and Cox, D.D. (2009). A rodent model for the study of invariant visual object recognition. Proceedings of the National Academy of Science, U.S.A., 106, 8748-8753. [50] Wortwein, G., Morgensen, J., Williams, G., Carlos, J.H., and Divac, I. (1994) Cortical area in the rat that mediates visual pattern discrimination.
Acta Neurobiologiae
Experimentalis, 54, 365 - 376. [51] Eacott, M.J., Machin, P.E., and Gaffan, E.A. (2001). Elemental and configural visual discrimination learning following lesions to perirhinal cortex in the rat. Behavioural Brain Research, 124, 55 - 70.
16
Lateral masking effects in rats Figure Captions
Figure 1. A. Top view displaying geometry of test chamber. Test stimuli (Gabor patches) appeared on the monitor, subtending a visual angle of either 5.9° or 14.0°. B. Trial events and reaction time measurements. Dotted lines represent variable ranges of events. Test stimulus onset relative to initial nose-poke occurred with a randomly chosen latency, ranging from 500 – 2000 ms.
17
Lateral masking effects in rats Figure 2. Reaction Time Cluster Index. A. Reaction time frequency distribution was first compiled for trials with no stimuli. The upper boundary of the no-stimulus (nominal) distribution was set to 2 S.D. above the mean. B. For each contrast level, response frequencies above the nominal boundary served as the cluster index.
18
Lateral masking effects in rats Figure 3. A. Stimuli at five levels of contrast, as well as no-stimulus condition (right-most display). B. Boundaries of nominal distribution (±2 S.D.) are depicted with gray field. Examples of responses above nominal are shown for each level of contrast.
19
Lateral masking effects in rats Figure 4. For targets alone, A. response index (frequency distribution above that found for no-stimulus condition) across contrast, fitted to sigmoidal functions.
Threshold
contrast, derived from response indices of 2.5%, are depicted for each stimulus condition. B. Contrast sensitivity for each spatial frequency tested.
20
Lateral masking effects in rats Figure 5. Response indices across contrast for targets alone, or targets with lateral masks. Error bars represent 1 SEM. Asterisks indicate significant differences between no mask and mask conditions.
21
Lateral masking effects in rats Figure 6. Contrast sensitivity for target alone or in the presence of lateral masks.
22
Lateral masking effects in rats Figure 7. Stimulus conditions and corresponding cluster index as a function of contrast. A and B: Collinear and orthogonal flankers for 0.21 cpd stimuli. C and D: Collinear and orthogonal flankers for 0.40 cps stimuli. E and F: Flanker separation of 5.2, 8.4, and 11.8 cycles.
23
S0166-4328(17)30573-9 http://dx.doi.org/doi:10.1016/j.bbr.2017.07.046 BBR 11018
To appear in:
Behavioural Brain Research
Received date: Revised date: Accepted date:
2-4-2017 11-7-2017 29-7-2017
Please cite this article as: Kurylo Daniel D, Yeturo Sowmya, Lanza Joseph, Bukhari Farhan.Lateral Masking Effects on Contrast Sensitivity in Rats.Behavioural Brain Research http://dx.doi.org/10.1016/j.bbr.2017.07.046 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
Lateral masking effects in rats 8/5/2017
Lateral Masking Effects on Contrast Sensitivity in Rats Daniel D. Kurylo1, Sowmya Yeturo1, Joseph Lanza1, and Farhan Bukhari2 1 Department
of Psychology, Brooklyn College CUNY, Brooklyn, NY 11210
2 Department
of Computer Science, The Graduate Center CUNY, New York, NY 10016
Corresponding author: Daniel D. Kurylo Psychology Department Brooklyn College CUNY 2900 Bedford Avenue Brooklyn, NY 11210
Phone: 718-951-5000 x 6022 Fax: 718-951-4814 e-mail: [email protected]
Highlights
Visual contrast sensitivity in rats is reduced by adjacent, non-overlapping masks
Lateral mask effects were unaffected by relative orientation or separation of masks
Results are consistent with non-systematic orientation topography in rodent cortex
Abstract Changes in target visibility may be produced by additional stimulus elements at adjacent locations.
Such contextual effects may reflect lateral interactions of stimulus
representations in early cortical areas. It has been reported that the organization of orientation preference found in primates and cats visual cortex differs from that found in rodents, suggesting functional distinctions across species. In order to examine effects of
1
Lateral masking effects in rats lateral interactions at a perceptual level, contrast sensitivity in rats was measured for Gabor patches masked by two additional patches. Rats responded to target onset, and perceptual indices were based upon reaction time distributions across levels of luminance contrast.
It was found that contrast sensitivity of targets without lateral masks
corresponded to levels previously reported. For all measurements, the presence of sustained lateral masks systematically reduced sensitivity to targets, demonstrating interference by adjacent elements across levels of contrast. Effects of mask orientation or separation were not observed. These results may reflect reported non-systematic topography of orientation tuning across the cortex in rodents. Results suggest that intrinsic lateral connections in early processing areas play a minimal role in stimulus integration for rats.
keywords: animal perception; animal psychophysics; visual cortex; cortical integration; lateral flankers
1. Introduction
Visibility of stimulus components may be enhanced or diminished by the presence of adjacent stimulus elements. Such effects are evident with high-contrast lateral masks [1], metacontrast with zero stimulus onset asynchrony [2], and crowding of peripheral targets [3]. Contextual effects on perceptual capacities may reflect neural interactions among representations of targets and lateral masks. At a neural level, response properties of cortical neurons are modulated by the context in which stimuli are placed [4,5,6]. In primates and cats, systematic relationships exist among the orientation preference of neurons. Such connections may contribute to a system of enhancement and inhibition of signals based upon contextual effects from other cortical sites [7,8]. In rodents, the distribution of orientation preference is not systematic [9,10], nor do lateral projections display the periodic patches found in primates and cats [11]. These distinctions in cortical organization suggest that lateral interactions among stimulus elements may operate differently in rats than in primates and cats.
2
Lateral masking effects in rats At a perceptual level, the ability of rats to discriminate the presence or absence of targets declined when target onset was accompanied by flankers [12]. In addition, misses as well as false alarms increased when flankers were collinear to targets, compared to flankers that deviated from collinearity. Such effects on detecting suprathreshold stimuli were observed across a range of contrasts of both targets and flankers [13]. For humans, contrast thresholds are elevated in the presence of collinear, co-axial Gabor patches positioned near test stimuli (within 2 cycles), whereas thresholds decrease with adjacent elements positions within a farther zone (approximately 3 – 10 cycles) [14]. Flanker effects appear to be restricted to near foveal viewing [15,16] to which attention is directed [17,16], and are not observed at suprathreshold levels [15]. Flanker effects may reflect a system for contour integration mediated by short- and long-range interactions within neural populations [18]. The functional significance of connection patterns in local cortical circuits may be distinguished across species [19]. In order to explore lateral masking on detection thresholds in rats, responses to target onset were measured across luminance contrast for targets presented alone, or in the presence of masks.
2. Methods
2.1. Subjects Ten Long-Evans hooded rats served as subjects, each randomly assigned to one or more stimulus conditions. Animals were deprived of water for 22 hours before each session, and allowed water ad lib for one hour following sessions. Sessions occurred five days each week, and animals were allowed water ad lib on the remaining two days. This study was conducted in accordance with the National Institutes of Health Guide for the Care and Use of Laboratory Animals, and approved by the Institutional Animal Care and Use Committee of Brooklyn College. 2.2. Apparatus Behavioral measurements were made in a customized operant conditioning chamber (Figure 1A). The front panel of the chamber supported a metal funnel that extended 3 cm outside of the chamber. Animals had access to the funnel through a 5 cm diameter
3
Lateral masking effects in rats hole, centered 2.5 cm from the chamber floor. Placement of the rat's head completely within the funnel disrupted an infrared (IR) light beam connecting an emitter/detector pair mounted at the tip of the funnel. Rats viewed the stimulus through holes in the funnel positioned over each eye. Viewing stimuli from the head-fitted funnel allowed control over viewing position across trials. Rats had access to an enclosed drinking well positioned next to the funnel. A measured amount of water was delivered to the drinking well by means of a solenoid driven valve. Circuitry for the IR pair and solenoid were interfaced via solid-state relay switches to a computer. Stimulus generation, data collection, and trial events were controlled in real-time by customized computer software [20].
2.3. Stimulus Presentation In an otherwise darkened room, stimuli were presented on a computer monitor (Trinitron CPD 4401) controlled by a graphics adaptor (NVidia GeForce FX5200) set to 1280 x 1024 pixel resolution. Rats viewed stimuli at a distance of 24 cm and elevated by 10°, centered within the binocular region of the visual field. Stimuli consisted of Gabor patches on a gray background (22.3 cd/m2). Luminance levels were linearized across a range of 2.9 to 42.2 cd/m2.
2.4. General Procedure Using a free-operant procedure, rats initiated trials by placing their head into a central funnel. Following a delay, generated randomly between 500 and 2000 ms, a Gabor patch appeared on the monitor. Rats were trained to remain stationary until stimulus onset, to which they responded by withdrawing their head from the funnel (Figure 1B). Following training, data collection occurred on approximately every other session. In order to maintain consistence performance, a session of maintenance training occurred on alternate days.
2.5. Training Procedure
4
Lateral masking effects in rats Following initial magazine training, rats were trained to nose-poke the central funnel. The next phase of training required rats to remain stationary in the funnel for increasing lengths of time, culminating with a 500 ms hold period. A high-contrast Gabor patch was presented on the monitor at the end of the required hold period. For the next phase of training, stimulus onset varied randomly between 500 - 750 ms, and rats were required to withdraw their head from the funnel within 750 ms of stimulus onset. Across training sessions, stimulus onset times progressively increased to 500 - 2000 ms, and reaction time to stimulus onset was progressively restricted to 50 - 400 ms. Progressive increase to stimulus onset range, and progressive decrease in reaction time window, was contingent upon rats' performance, requiring 90% correct across a single session. For data collection sessions, reward was delivered on each trail, regardless of reaction time. In order to maintain conditioning, each session of data collection was followed by a training session.
2.6. Reaction Time Cluster Index Reaction time was recorded from stimulus onset to head withdrawal. Frequency distributions of reaction times, time-locked to stimulus onset, were displayed as histograms. High-contrast stimuli produced reaction time distributions that clustered about a mean of 237 ms (S.D. 104 ms). Given the unpredictable onset time of stimuli, the clustering pattern of reaction time distributions verified behavioral control by the stimulus. Quantification of reaction time clustering was based upon the incidence of responses that occurred above that found on no-stimulus trials. Specifically, the distribution of response frequency (histogram bin height) across reaction time was first determined for no-stimulus trials (Figure 2A). The upper boundary of the nominal distribution was set to 2 S.D. above the distribution mean. Reaction time distributions were then measured for each stimulus condition (Figure 2B). For each contrast level, the sum of response frequencies above the nominal boundary served as the response index.
5
Lateral masking effects in rats 2.7. Psychophysical Measurements Detection thresholds were determined with the psychophysical Method of Constant Stimuli. For each condition, reaction time distributions were compiled for each of six contrasts, as well as a no-stimulus condition, presented in random order across trials. No-stimulus trials were therefore randomly interleaved among the stimulus-present trials. For each contrast level, reaction time distributions were based upon approximately 150 trials, collected across multiple sessions. For no-stimulus trials, reaction times were calculated from a randomized presentation time (between 500 - 2000 ms from trial initiation), thereby corresponding to conditions for the stimulus-present trials. Examples of reaction time frequency distributions across contrast are depicted in Figure 3. For high-contrast stimuli, response frequency above the nominal boundary was approximately 25%, and progressively declined with reduced contrast. Response indices, plotted across contrast, are described well by a sigmoidal function. Threshold contrast, extrapolated from the sigmoidal function, was set to a response index of 2.5%. This value corresponds to the initial elevation in the psychometric function.
2.8. Stimulus Conditions Contrast thresholds were measured for targets alone, or in the presence of masks that varied in orientation and lateral separation.
2.8.1. Contrast Sensitivity. Contrast sensitivity was determined for 0.21 cpd, which corresponds to near peak sensitivity for Long-Evans rats [21,23], and 0.40 cpd, which corresponds to approximately the midpoint of the high-frequency limb of the CSF. The 0.21 cpd patch subtended a visual angle of 14.0°, in which approximately 2.5 cycles were visible.
The 0.40 cpd patch was presented at two sizes, 14.0° and 5.9°, in which
approximately 5.5 and 2.5 cycles were visible, respectively.
2.8.2. Lateral Mask. For the lateral mask condition, masks, set to a Michelson contrast of 0.53, were positioned above and below test stimuli. In all cases, lateral masks
6
Lateral masking effects in rats matched test stimuli spatial frequency and size. For the 0.21 cpd condition, lateral masks were positioned 2.8 cycles from test stimuli centers. For the 0.40 cpd condition, lateral masks were positioned 5.7 (for patch size 14.0°) and 2.8 cycles (for patch size 5.9°) from test stimuli. Lateral masks existed before rats placed their head into the funnel, and remained visible throughout the trial. Rats thereby responded to the onset of test stimuli, without additional cues introduced by mask onset.
2.8.3. Lateral Mask Orientation.
To investigate effects of relative orientation,
performance was compared between lateral masks that were collinear or orthogonal to test stimuli. Orientation effects were examined for 0.21 and 0.40 cpd, with a patch size of 14.0°.
2.8.4. Lateral Mask Separation. To investigate effects of lateral mask separation, performance was compared across lateral masks positioned 2.8, 4.8, and 6.8 cycles from test-stimulus centers. Separation effects were examined for the 0.21 cpd, 5.9° size condition. In all cases, lateral masks were collinear to test stimuli.
3. Results
For high-contrast stimuli, response indices reached approximately 25%, although some rats did not reach this level even with the maximum contrast. In order to equate variation in behavioral patterns across rats, response indices were normalized to 25%. For each condition, response indices as a function of contrast were determined separately for each rat. Best-fit sigmoidal functions were then determined for each rat, from which 2.5% thresholds were extrapolated. Statistical analyses were then applied to response thresholds.
3.1. Contrast Sensitivity. Mean response indices are depicted for each condition (Figure 4). A sigmoidal function fit to response indices is also shown in order to demonstrate the response
7
Lateral masking effects in rats pattern.
Mean contrast threshold at 0.21 cpd was 7% (Michelson), and contrast
thresholds at 0.40 cpd were 13% and 18% for the large and small targets, respectively. For large targets, contrast thresholds differed significantly between 0.21 and 0.40 cpd (Mann-Whitney U = 0, p < .05). Contrast thresholds for the two target sizes at 0.40 cpd also differed significantly (U = 0, p < .05). Examining performance across contrast, responses at 0.21 and 0.40 cpd differed significantly (p < .05). A trend existed across intermediate contrasts for the size factor at 0.40 cpd, although differences reached significance only for 22% contrast.
3.2. Lateral Mask Effects. Mean response indices across contrast, with best-fit functions, are displayed in Figure 5. Performance with masks was reduced compared to targets alone for intermediate levels of contrast. Specifically, for the 0.21 cpd condition, performance with masks differed significantly from target alone for contrasts between 16 - 28% (U = 1.5 at each contrast; p < 0.05). For 0.40, 14.0° condition, masks vs. target alone conditions differed significantly for contrasts between 16 - 36% (across contrasts U ranged from 1.00 to 2.5 ; p < 0.05). For the 0.40 cpd, 5.9° condition, masks and target alone conditions differed significantly for contrasts between 16 - 22% (U ranged from 1.00 to 2.00; p < 0.05). Comparing contrast sensitivity, lateral masks reduced sensitivity for each of the stimulus conditions (Figure 6). Sensitivity with masks was significantly lower than with target alone for the 0.21 cpd (U = 4.00; p < 0.05), 0.40 cpd, 14.0° (U = 5.50; p < 0.05), and 0.40 cpd, 5.9° (U = 5.50; p < 0.05) conditions.
3.3. Orientation Effects Performance was similar for collinear and orthogonal masks for both the 0.21 (Figure 7B) and 0.40 cpd conditions (Figure 7D). Comparing performance at each level of
8
Lateral masking effects in rats contrast, collinear and orthogonal mask conditions did not differ significantly for either the 0.21 or 0.44 cpd conditions (Mann-Whitney, p > 0.05).
3.4. Separation Effects Performance was similar for mask separations of 5.2, 8.4, and 11.8 cpd (Figure 7F). Comparing results at each level of contrast, performance did not differ significantly across levels of mask separation (Kruskal-Wallis, p > 0.05).
4. Discussion
These results demonstrate a masking effect in rats on contrast sensitivity by stimuli positioned at adjacent, non-overlapping positions. In this regard, lateral interactions of stimulus components are apparent at a perceptual level. As with suprathreshold stimuli [12,13], contrast thresholds in rats are elevated in the presence of lateral masking. Contrast sensitivities reported here for target alone are similar to previous studies, although sensitivity measurements reported here are greater than those from previous reports [21,22,23]. Differences may reflect distinctions in stimulus parameters, including wave pattern, target size, and mean luminance, as well as psychophysical techniques. In addition, head position was regulated in the current study in order to preclude introducing additional visual cues. Free moving rats may introduce visual cues produced by lateral head movements that reduce the ability to specify parameters such as luminance or spatial frequency [24]. Similarly, specifying stimulus metrics, including luminance and spatial frequency, requires regulation of stimulus position relative to the corneal surface [25,26,27]. Nevertheless, limitations in psychophysical measures in rats may obscure perceptual effects, such that sensitivity differences across masking conditions may be less than measurement resolution. In addition, because flanker effects on contrast thresholds are restricted to regions near the fovea [15,16], eye position, which is not controlled in rat measurements, may affect sensitivity. This issue may be further complicated by retinal characteristics of rats, in which area centralis and farther eccentric regions encode stimuli at a lower sampling density than occurs with primate foveal fixation [28,29].
9
Lateral masking effects in rats Performance did not differ significantly between relative orientation or among levels of separation. These results differ from those of Meier et al. [12], where flanker orientation affected target detection. Whereas some aspects of stimulus presentation were similar to those used here, significant procedural differences may account for differences in results. Procedures employed by Meier et al. allowed measures of response choice across levels of stimulus configurations. Rats made a two-alternative forced-choice response indicating "yes" or "no" to the presence of the target. Increased missed targets and increased false alarm rates occurred when targets and flankers were collinear, compared to misalignment conditions. In contrast, target detection measured here was based upon the reaction time distribution relative to the onset of the target. Across trials, flankers were either not presented, or had been visible before trials were initiated. Procedural differences between the studies may affect response factors, including perceptual decision. Although procedures used here allow high sensitivity to target detection, they may not allow sufficient measurement resolution to distinguish performance across differences in relative orientation of targets and flankers.
4.1. Mechanisms of integration. Differences in perceptual capacities across species may be associated with neural circuitry in early visual areas. In primates and cats, V1 topography displays a systematic pattern of orientation preference [30,31,32]. In addition, relative neural responses are enhanced by stimuli in adjacent areas that match a cell's orientation preference, and suppressed by stimuli that deviate from the preferred orientation [4,33,34,35]. In rats, a proportion of cells in primary visual cortex are selective for orientation [36,37,38,9]. Horizontal neural connections, found mainly in layers 2/3 and 5, project laterally within the same layer [39,40,41] as well as crossing layers [42]. Horizontal connections in rats extend laterally to 2 mm [40,41], linking neurons with overlapping receptive fields [39]. However, rodents display a heterogeneity of orientation preference in early cortical areas [9,10]. The absence of orientation effects reported here may reflect the locally disordered topography of orientation preference. As such, characteristics of local cortical connections in rats may be reflected at a perceptual level. Integration of stimulus elements in rats may be less associated with intrinsic lateral connections in early cortical areas, and more with long-range interactions, such as convergence across visual areas. Cortical mediation of pattern perception in rats is associated with both striate and lateral prestriate cortex [43,44,45]. Cortical areas in rats receive retinal input from two pathways, one passing from dorsal lateral geniculate
10
Lateral masking effects in rats nucleus to striate cortex, the other passing from superior colliculus to lateral posterior nucleus of the thalamus, and on to medial and lateral prestriate cortex and higher cortical areas [24,46,47]. The alternate pathway includes connections that bypass primary cortex, providing input to high-order areas not dependent on subordinate processing in striate cortex. Higher levels of processing that contain larger receptive fields perform more global analyses of stimuli, and are therefore well suited for integrating forms. Rats are capable of object recognition with transformation of stimulus characteristics, such as size, rotation, or position [48,49]. Systematic analysis of stimulus components indicates that recognition in rats is based upon integrating a pattern of object features, as opposed to a specific low-level stimulus characteristic [25]. In rats, lesions to areas 35 and 36, which show functional similarities to primate inferotemporal cortex [50], disrupt discrimination involving the conjunctions of features, suggesting that these regions contain configural representations of stimuli [51]. Pattern regularities among stimulus elements may thereby be processed at later stages, in which global relationships among stimulus components are encoded. Acknowledgements This work was supported by the City University of New York PSC-CUNY Research Award Program.
11
Lateral masking effects in rats References [1] Polat, U., and Sagi, D. (1994). The architecture of perceptual spatial interactions. Vision Research, 34, 73-78. [2] Breitmeyer, B., and Ganz, L. (1976). Implications of sustained and transient channels for theories of visual pattern masking, saccadic suppression, and information processing. Psychological Review, 83, 1-36. [3] Grainger, J., Tydgat, I., and Issele, J. (2010). Crowding affects letters and symbols differently.
Journal of Experimental Psychology, Human Perception and
Performance, 36, 673-688. [4] Angelucci, A., Levitt, J.D., Walton, E.J., Hupe, J.M., Bullier, J., and Lund, J.S. (2002b). Circuits for local and global integration in primary visual cortex.
Journal of
Neuroscience, 22, 8633-8646. [5] Bringuier, V., Chavane, F., Glaeser, L., and Fregnac, Y. (1999).
Horizontal
propagation of visual activity in the synaptic integration field of area 17 neurons. Science, 283, 695-699. [6] Kapadia, M.K., Ito, M., Gilbert, C.D. and Westheimer, G. (1995). Improvement in visual sensitivity by changes in local context: parallel studies in human observers and in V1 of alert monkeys. Neuron, 15, 843-856. [7] Alonso, J.M. (2002). Neural connections and receptive field properties in the primary visual cortex. Neuroscientist, 8, 443-456. [8] Angelucci, A., Levitt, J.D., Lund, J.S. (2002a). Anatomical origins of the classical receptive field and modulatory surround field of single neurons in macaque visual cortical area V1. Progress in Brain Research 136, 373-388. [9] Ohki, K., Chung, S., Ch'ng, Y.H., Kara, P., and Reid, R.C. (2005). Functional imaging with cellular resolution reveals precise microarchitecture in visual cortex. Nature, 433, 597-603. [10] Van Hooser, S.D., Heimel, J.A., Chung, S., Nelson, S.B., and Toth, L.J. (2005). Orientation selectivity without orientation maps in visual cortex of a highly visual mammal. Journal of Neuroscience, 25, 19-28.
12
Lateral masking effects in rats [11] Van Hooser, S.D., Heimel, J.A., Chung, S., and Nelson, S.B. (2006). Lack of patchy horizontal connectivity in primary visual cortex of a mammal without orientation maps. Journal of Neuroscience, 26, 7680 – 7692. [12] Meier, P., Flister, E., and Reinagel, P. (2011). Collinear features impair visual detection by rats. Journal of Vision, 11, 119-122. [13] Meier, P., and Reinagel, P. (2013). Rats and humans differ in processing collinear visual features. Frontiers in Neural Circuits, 7, 1-8. [14] Polat, U., and Sagi, D. (1993). Lateral interactions between spatial channels: suppression and facilitation revealed by lateral masking experiments.
Vision
Research, 33, 993-999. [15] Williams, C.B., and Hess, R.F. (1998). Relationship between facilitation at threshold and suprathreshold contour integration. Journal of the Optical Society of America, 15, 2046-2051. [16] Shani, R., and Sagi, D. (2005). Eccentricity effects on lateral interactions. Vision Research, 45, 2009-2024. [17] Freeman, E., Sagi, D., and Driver, J. (2001). Lateral interactions between targets and flankers in low-level vision depend on attention to the flankers.
Nature
Neuroscience, 4, 1032-1036. [18] Andini, Y., Sagi, D., and Tsodyks, M. (1997). Excitatory-inhibitory networks in the visual cortex: psychophysical evidence. Proceedings from the National Academy of Science, 94, 10426-10431. [19] Kaschube, M. (2014). Neural maps versus salt-and-pepper organization in visual cortex. Current Opinion in Neurobiology, 24, 95-102. [20] Bukhari, F., and Kurylo, D.D. (2008). Computer programming for generating visual stimuli. Behavior Research Methods, 40, 38-45. [21] Birch, D. & Jacobs, G.H. (1979). Spatial contrast sensitivity in albino and pigmented rats. Vision Research, 19, 933-937. [22] Legg, C.R., and Turkish, S. (1983).
Spatial contrast sensitivity changes after
subcortical visual system lesions in the rat. Behavioural Brain Research, 7, 253-259. [23] Legg, C.R. (1984). Contrast sensitivity at low spatial frequencies in the hooded rat. Vision Research, 24, 159-161.
13
Lateral masking effects in rats [24] Dean, P. (1990). Sensory Cortex: Visual Perceptual Functions. In B Kolb RC Tees (eds), The Cerebral Cortex of the Rat. Cambridge, MA: MIT Press, pp. 275-307. [25] Alemi-Neissi, A., Rosselli, F.B., and Zoccolan, D. (2013).
Multifeatural shape
processing in rats engaged in invariant visual object recognition.
Journal of
Neuroscience, 33, 5939-5956. [26] Kurylo, D.D. (2008). Effects of visual cortex lesions on perceptual grouping in rats. Behavioural Brain Research, 190, 182-188. [27] Kurylo, D.D., Van Nest, J., and Knepper, B. (1997). Characteristics of perceptual grouping in rats. Journal of Comparative Psychology, 111, 126-134. [28] Cowey, A., Franzini, C. (1979). The retinal origin of uncrossed optic nerve fibers in rats and their role in visual discrimination. Experimental Brain Research, 35, 443– 455. [29] Cowey, A., and Perry, V.H. (1979). The projection of the temporal retina in rats, studied by retrograde transport of horseradish peroxidase.
Experimental Brain
Research, 35, 457-464. [30] Blasdel, G.G., and Salama, G. (1986). Voltage-sensitive dyes reveal a modular organization in monkey striate cortex. Nature, 321, 579-585. [31] Grinvald, A., Lieke, E., Frostig, R.D., Gilbert, C.D., and Wiesel, T.N. (1986). Functional architecture of cortex revealed by optical imaging of intrinsic signals. Nature, 324, 361-364. [32] Polimeni. J.R., Granquist-Fraser D., Wood R.J., and Schwartz E.L. (2005). Physical limits to spatial resolution of optical recording: clarifying the spatial structure of cortical hypercolumns. Proceedings of the National Academy of Science, U S A, 102, 41584163. [33] Bosking, W.H., Zhang, Y., Schofield, B., and Fitzpatrick, D. (1997). Orientation selectivity and the arrangement of horizontal connections in tree shrew striate cortex. Journal of Neuroscience, 17, 2112-2127. [34] Crook, J.M., Engelmann, R., and Löwel, S. (2002). GABA-inactivation attenuates collinear facilitation in cat primary visual cortex. Experimental Brain Research, 143, 295-302.
14
Lateral masking effects in rats [35] Kasamatsu, T., Polat, U., Pettet, M.W., Norcia, A.M. (2001). Colinear facilitation promotes reliability of single-cell responses in cat striate cortex. Experimental Brain Research, 138, 163-172. [36] Parnavelas, J.G., Burne, R.A., and Lin, C.S. (1981). Receptive field properties of neurons in the visual cortex of the rat. Neuroscience Letters, 27, 291-296. [37] Girman, S.V., Sauve, Y., and Lund, R.D. (1999). Receptive field properties of single neurons in rat primary visual cortex. Journal of Neurophysiology, 82, 301-311. [38] Wiesenfeld, Z., and Kornel, E.E. (1975). Receptive fields of single cells in the visual cortex of the hooded rat. Brain Research, 94, 401-412. [39] Rumberger, A., Tyler, C.J., Lund., J.S. (2001). Intra- and inter-areal connections between the primary visual cortex V1 and the area immediately surrounding V1 in the rat. Neuroscience, 102, 35 - 52. [40] Burkhalter, A, and Charles, V. (1990). Organization of local axon collaterals of efferent projections neurons in rat visual cortex. Journal of Comparative Neurology, 302, 920 - 934. [41] Telfeian, A.E., and Connors, B.W. (2003). Widely integrative properties of layer 5 pyramidal cells support a role for processing of extralaminar synaptic input in rat neocortex. Neuroscience Letters, 343, 121-124. [42] Ichinose T Murakoshi T (1996). Electrophysiological elucidation of pathways of intrinsic horizontal connections in the rat visual cortex. Neurosci, 73, 25 - 37. [43] McDaniel, W.F., Coleman, J., and Lindsay Jr, J.F. (1982). A comparison of lateral peristriate and striate neocortical ablations in the rat. Behavioural Brain Research, 6, 249-272. [44] McDaniel, W.T., and Nobel, L.M. (1984). Visual pattern discrimination following bilateral striate or lateral peristriate neocortical injuries. IRCS Journal of Medical Science, 12, 1084-1085. [45] Lindsay, J.F., and McDaniel, W.F. (1987). Neural tissue transplants in rats with lateral peristriate lesions: II Behavior. Med Sci Res, 15, 655-656. [46] Sefton, A.J., and Dreher, B. (1985). Visual System In G Paxinos (ed), The Rat Nervous System, Vol 1 Forebrain and Midbrain. Sydney: Academic Press, , pp. 169221.
15
Lateral masking effects in rats [47] Zarrinpar, A., and Callaway, E.M. (2006). Local connections to specific types of layer 6 neurons in the rat visual cortex. Journal of Neurophysiology, 95, 1751-1761. [48] Tafazoli, S., Di Filippo, A., and Zoccolan, D. (2012). Transformation-tolerant object recognition in rats revealed by visual priming. Journal of Neuroscience, 32, 21-34. [49] Zoccolan, D., Oertelt, N., DiCarlo, J.J., and Cox, D.D. (2009). A rodent model for the study of invariant visual object recognition. Proceedings of the National Academy of Science, U.S.A., 106, 8748-8753. [50] Wortwein, G., Morgensen, J., Williams, G., Carlos, J.H., and Divac, I. (1994) Cortical area in the rat that mediates visual pattern discrimination.
Acta Neurobiologiae
Experimentalis, 54, 365 - 376. [51] Eacott, M.J., Machin, P.E., and Gaffan, E.A. (2001). Elemental and configural visual discrimination learning following lesions to perirhinal cortex in the rat. Behavioural Brain Research, 124, 55 - 70.
16
Lateral masking effects in rats Figure Captions
Figure 1. A. Top view displaying geometry of test chamber. Test stimuli (Gabor patches) appeared on the monitor, subtending a visual angle of either 5.9° or 14.0°. B. Trial events and reaction time measurements. Dotted lines represent variable ranges of events. Test stimulus onset relative to initial nose-poke occurred with a randomly chosen latency, ranging from 500 – 2000 ms.
17
Lateral masking effects in rats Figure 2. Reaction Time Cluster Index. A. Reaction time frequency distribution was first compiled for trials with no stimuli. The upper boundary of the no-stimulus (nominal) distribution was set to 2 S.D. above the mean. B. For each contrast level, response frequencies above the nominal boundary served as the cluster index.
18
Lateral masking effects in rats Figure 3. A. Stimuli at five levels of contrast, as well as no-stimulus condition (right-most display). B. Boundaries of nominal distribution (±2 S.D.) are depicted with gray field. Examples of responses above nominal are shown for each level of contrast.
19
Lateral masking effects in rats Figure 4. For targets alone, A. response index (frequency distribution above that found for no-stimulus condition) across contrast, fitted to sigmoidal functions.
Threshold
contrast, derived from response indices of 2.5%, are depicted for each stimulus condition. B. Contrast sensitivity for each spatial frequency tested.
20
Lateral masking effects in rats Figure 5. Response indices across contrast for targets alone, or targets with lateral masks. Error bars represent 1 SEM. Asterisks indicate significant differences between no mask and mask conditions.
21
Lateral masking effects in rats Figure 6. Contrast sensitivity for target alone or in the presence of lateral masks.
22
Lateral masking effects in rats Figure 7. Stimulus conditions and corresponding cluster index as a function of contrast. A and B: Collinear and orthogonal flankers for 0.21 cpd stimuli. C and D: Collinear and orthogonal flankers for 0.40 cps stimuli. E and F: Flanker separation of 5.2, 8.4, and 11.8 cycles.
23