Report. A Specialized Area in Limbic Cortex for Fast Analysis of Peripheral Vision

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1 Current Biology 22, , July 24, 2012 ª2012 Elsevier Ltd All rights reserved DOI /j.cub A Specialized Area in Limbic Cortex for Fast Analysis of Peripheral Vision Report Hsin-Hao Yu, 1, * Tristan A. Chaplin, 1 Amanda J. Davies, 1,2 Richa Verma, 1 and Marcello G.P. Rosa 1,2 1 Department of Physiology 2 Monash Vision Group Monash University, Clayton, Victoria 3800, Australia Summary In primates, prostriata [1 3] is a small area located between the primary visual cortex (V1) and the hippocampal formation. Prostriata sends connections to multisensory and high-order association areas in the temporal, parietal, cingulate, orbitofrontal, and frontopolar cortices [4 14]. It is characterized by a relatively simple histological organization, alluding to an early origin in mammalian evolution. Here we show that prostriata neurons in marmoset monkeys exhibit a unique combination of response properties, suggesting a new pathway for rapid distribution of visual information in parallel with the traditionally recognized dorsal and ventral streams. Whereas the location and known connections of prostriata suggest a high-level association area, its response properties are unexpectedly simple, resembling those found in early stages of the visual processing: neurons have robust, nonadapting responses to simple stimuli, with latencies comparable to those found in V1, and are broadly tuned to stimulus orientation and spatiotemporal frequency. However, their receptive fields are enormous and form a unique topographic map that emphasizes the far periphery of the visual field. These results suggest a specialized circuit through which stimuli in peripheral vision can bypass the elaborate hierarchy of extrastriate visual areas and rapidly elicit coordinated motor and cognitive responses across multiple brain systems. Results Prostriata is a small, distinct area located in a bridge of cortex that links the retrosplenial and parahippocampal regions (Figure 1A). Like these limbic cortices, prostriata lacks the clear six-layered cellular structure that characterizes the majority of the cerebral cortex, and is lightly myelinated (see Figure S1 available online). However, we found that prostriata is unlike other limbic cortices in that its neurons consistently show robust responses to visual stimulation. Prostriata Neurons Have Short Response Latencies but Enormous Receptive Fields We explored the responses of neurons in prostriata to visual stimuli, using single-unit recordings in marmoset monkeys. Recording sites were reconstructed relative to electrolytic lesions and histological boundaries (Figure S1). As expected [15], neurons near the rostral boundary of V1 had receptive fields in the far periphery of the visual field (Figures 1B and 1C). Crossing the histological boundary into prostriata *Correspondence: hhyu00@gmail.com resulted in a clear-cut change in visual response properties. Among the most notable features, the receptive fields became much larger (>30 in length) and much less selective to direction of motion and orientation (Figures S1 and S4). A flashed patch of light was an effective stimulus for the vast majority (>90%) of prostriata neurons, allowing precise mapping of receptive fields. The responses were robust and consistent upon repeated stimulations, showing little sign of adaptation (Figure 2A; Figure S2). Using this stimulation, we compared the response properties of neurons in prostriata (n = 90) and in the far peripheral representation of V1 (n = 78). This analysis yielded three key observations. First, prostriata neurons had higher spontaneous firing rates than V1 neurons (13.9 Hz versus 3.8 Hz; one-sided Mann-Whitney test, U = 6,786, p < 0.01). Second, the median response strength (Figure 2B) was similar in prostriata and V1 (46.7 Hz versus 39.7 Hz; Mann-Whitney test, U = 4,128.5, p = 0.426). Third, the response onset latencies observed in prostriata were comparable to those observed in peripheral V1 under similar conditions (Figure 2C; Figure S2). The distribution of response latencies in prostriata suggested the possibility of two neuronal populations (Dip test of uniformity: D = 0.05, p = 0.034). Nonetheless, the distributions of latencies observed in these areas covered the same range (V1: ms; prostriata: ms) and had similar median values (55 ms versus 56 ms; Mann-Whitney test, U = 3,574, p = 0.840). Whenever tested, cells with receptive fields in the binocular part of the visual field responded to stimulation of either eye. We obtained receptive field maps of 73 prostriata neurons using a flashed square projected to locations on a grid (Figure 3). The receptive fields were typically not circularly symmetrical, and the strongest responses were often obtained away from their geometrical centers. The median width and length of the receptive fields in our sample were 29.9 and 49.1, respectively (Figure 3E); even the smallest receptive field (centered 60.9 from the fovea) was 25.3 long. On average, the area covered by each receptive field corresponded to 10% of the contralateral hemifield (Figure 3F; Figure S3). Notably, unlike in any other primate visual area described to date, there was no systematic relationship between eccentricity and receptive field area (Kendall s rank correlation coefficient t = , p = 0.367). The Representation of the Outer Limits of the Visual Field Is Emphasized in Prostriata In a unique pattern among all primate areas studied so far, most prostriata neurons had receptive fields centers (points of maximal response) at eccentricities (distances from the fovea) greater than 50 (Figure 3F). Nonetheless, when receptive borders were considered, they formed a complete representation of the contralateral hemifield (Figure S3). The representation of polar angle (angular deviation from the horizontal meridian of the visual field) was systematic, and congruent with that found in V1, but the representation of eccentricity was more irregular (Figures 1B and 1C). In general, neurons near the caudal border of prostriata with V1 had receptive field centers located in the far periphery of the visual field, and eccentricities decreased toward its rostral boundary. We

2 Current Biology Vol 22 No Figure 1. Location of Prostriata in the Marmoset Monkey and Its Visuotopic Organization (A) Ventromedial view of the layer-4 surface of the left hemisphere of a marmoset brain, showing the location of prostriata (ProSt) relative to surrounding cortical areas. Prostriata (red) is located near the rostral tip of the calcarine sulcus and is bounded dorsally by the retrosplenial cortex (area 23V, the ventral component of area 23, and area 30 [3]). The insert indicates the magnified region in relation to the rest of the brain. The abbreviations follow a recent review of the organization of the cerebral cortex of the marmoset [36]. (B) The polar angles of the centers of the excitatory receptive fields of 201 neurons (color-coded according to the wheel shown in the inset) recorded in prostriata and V1 in one animal. The recording sites are displayed on a computationally flattened reconstruction of the rostral part of the calcarine sulcus and adjacent retrosplenial cortex. Dashed lines indicate the histological boundaries of V1 and prostriata. The gray level represents the curvature of the cortex. Dark regions are concave (e.g., the fundus of the calcarine sulcus), and bright regions are convex. (C) The eccentricity of the receptive fields is shown in (B). Insert abbreviations: C, caudal; L, lateral; M, medial; R, rostral; D, dorsal; V, ventral. observed a distinct population of neurons (12/85; 14%) that responded to stimulation of two regions in the visual field, typically one central and the other peripheral (Figure 3D). Although it is possible that some of these responses may reflect recordings from two adjacent units, this relatively frequent observation reinforces the impression of an unusual visual topography.

3 Visual Function of Area Prostriata 1353 Prostriata Neurons Are Selective to Stimulus Speed, but Not Direction of Motion We used three types of visual stimuli to investigate the tuning properties of prostriata neurons: moving bars, kinetic dot fields, and sinusoidal drifting gratings. This analysis was based on 98 units with receptive fields centered between 40 and 70 eccentricity. Moving bars were the most effective type of stimulus, consistently eliciting higher response rates and more clearly defined tuning curves. We also experimented with other types of stimulus (e.g., looming disks and optical flow fields), but none of these proved more effective than simple moving bars. Prostriata neurons are poorly tuned to the orientation and direction of motion. One of the best-tuned units is illustrated in Figure 4A (see Figure S4 for additional examples). We used circular variance (cv) to quantify orientation selectivity [16]. Only 29.6% (29/98) of the neurons in our sample showed any hint of a bias in their responses to the orientation of moving bars (cv < 0.9). This is in contrast to the neighboring region of V1 (Figure 4B), where 74% of neurons showed orientation bias using the same criterion (median values: prostriata, cv = 0.93; V1, cv = 0.72; Mann-Whitney test, U = 14,213; p < 0.05). Only one prostriata neuron in our sample was strongly direction selective (direction index > 0.8). However, prostriata neurons exhibited clear tuning for the speed of the moving bar, with a distinct preference for very high speeds (Figure 4C; Figure S4). The median value of the optimal bar speed was /s (Figure 4D), and the median half-width half-height bandwidth value was 2.1 octaves. Figure 2. Responses of Prostriata Neurons to Brief Flashes of Uniform, Bright Stimuli (A) Raster diagram of the responses of a prostriata neuron to 80 consecutive flashes. The pink region indicates the time interval (0.2 s) during which the stimulus was present. The response pattern of this cell is summarized in the lower panel, which illustrates the peristimulus time histogram of the responses. The response onset latency (35 ms, indicated by the blue vertical line) was estimated using a maximal likelihood estimator of the change-point from spontaneous firing to stimulus-evoked responses [37]. The receptive field of this neuron (eccentricity 63 ) was 59 in diameter. The responses of several additional neurons to a similar test are illustrated in Figure S2. Prostriata Neurons Respond Well to Relatively Small and Sparse Stimuli We tested the selectivity of prostriata neurons to the length of bars presented at a near-optimal direction of motion and speed. Somewhat surprisingly, given the large receptive fields, the majority of neurons (68.4%, 67/98) showed little response modulation according to bar length. Among the 24 neurons that did show selectivity (24.5%), most increased their firing rate monotonically with length (Figure 4E). Using an integralof-gaussian model, the length summation field of the unit illustrated in Figure 4E was estimated to be 38.6, which was close to the size of the neuron s excitatory receptive field. Note, however, that much shorter bars could reliably activate this cell (half the above-baseline response was achieved using a 12.6 long bar). A small group of cells (7.1%, 7/98) showed statistically significant suppression in response to longer bars (Figure S4). Despite comprehensive tests employing variations of field diameter, direction of motion, speed, and density, kinetic dot fields proved to be less effective than bars, usually eliciting responses that were just above the spontaneous activity. Some prostriata neurons, however, did show selectivity to the density of dot fields (Figure 4F). In this test, the individual dots were 2 in diameter and moved at a speed of 100 /s. The optimal density was found to be as low as 4.2 dots per steradian, which amounted to only two or three dots moving within the entire receptive field at any time. Of 56 units that (B) Comparison of the response strength (peak spike rate in 10 ms bins above spontaneous rate) of neurons in prostriata (light gray) and in far peripheral V1 (dark gray). (C) Comparison of response latency of prostriata (light gray) and far peripheral V1 (dark gray) neurons. Arrowheads above histograms indicate the median values.

4 Current Biology Vol 22 No Figure 3. Quantification of the Geometry of Receptive Fields in Prostriata (A D) Examples of receptive fields mapped by a bright square projected at a grid of locations. The colors represent the mean above-spontaneous firing rates, normalized to the peak values. The contours in (A) (C) illustrate the shape of the receptive fields quantified by a model based on the bivariate skewed-normal distribution (equation 1 in Supplemental Experimental Procedures). The contours represent sensitivity at 30%, 50%, 70%, and 90% of the peak value. (D) An example of a receptive field showing two spatially distinct regions of activation. Longitudes and latitudes on the hemisphere are plotted in 10 intervals. The horizontal and the vertical meridians are indicated by thicker lines. (E) Distribution of the length and width of the receptive fields of 73 units, estimated from the best-fit functions as the region showing responses within 30% of the peak value. (F) Relationship between receptive field size and eccentricity in a sample of units for which quantitative receptive field maps were obtained. The receptive field size is expressed as the ratio of the surface area of the best-fit function and the surface area of the visual hemifield (p). The distributions of receptive field size and eccentricity of the receptive field center are plotted as histograms, with the arrowheads indicating median values. See Figure S3 for additional data. were tested for selectivity to the density of the dot fields, 48.2% (27/56) had clear preferences for very low densities; others showed little modulation (Figure S4). Prostriata Neurons Are Relatively Insensitive to Spatial and Temporal Modulation of the Stimuli Drifting sinusoidal gratings were generally ineffective stimuli. Most prostriata neurons responded transiently to the onset of the gratings but showed weak sustained responses. After removing initial transient responses from the spike trains, only 6 of 76 units (9.2%) were classified as simple using the F1/F0 > 1 criterion [17]. Thirty-nine neurons (51.3%) exhibited selectivity to spatial frequency (Figure S4), with a median preferred value that was much lower than that obtained in the far peripheral representation of V1 under similar conditions (0.03 c/ versus 0.14 c/ ). In addition, 46 neurons (60.5%) showed selectivity to temporal frequency; again, the median optimal value (1.4 Hz) was lower than that observed in V1 (4.0 Hz) [18]. Discussion Although reports of connections with visual areas [4 6] and responses to light [19 21] can be found scattered in the literature, there has been no study of the physiological properties of prostriata neurons. Prostriata has been traditionally regarded as a part of the retrosplenial limbic cortex [3]. Given the involvement of the retrosplenial cortex in memory, navigation, and other cognitive functions [22], it has been natural to expect that prostriata neurons exhibit physiological characteristics of higher-order association areas. This expectation was reinforced by tracer injection studies, which have demonstrated monosynaptic connections to a wide range of cortical systems, including not only visual [4 6], auditory [7, 8], and motor areas [2], but also association areas in the superior temporal [9], cingulate [10], parahippocampal [11], posterior parietal [7], medial prefrontal [12], orbitofrontal [13], and frontopolar [14] regions. Thus, the physiological properties of prostriata neurons revealed by our experiments were unexpected. These results indicate the existence of a significant, and yet unexplored anatomical bypass whereby peripheral vision can exert rapid and widespread effects over behavior and cognition. The response properties of prostriata neurons are highly unusual in light of expectations based on the hierarchical model of the organization of the visual cortex [23]. According to this model, as visual information is transmitted from V1 to areas at successively higher hierarchical levels, receptive fields become larger, response latencies longer, and stimulus selectivities more elaborate. Some of the response

5 Visual Function of Area Prostriata 1355 Figure 4. Tuning Characteristics of Prostriata Neurons (A) Direction tuning curves of a prostriata neuron, measured using a moving bar (solid line) and a kinetic dot field (dashed line). The speed of both stimuli was 100 /s. The curve measured with the moving bar is plotted in polar coordinates in the inset. This particular neuron (eccentricity was 70 ) was more selective than most of our samples (circular variance = 0.89). Tuning curves from eight additional cells are shown in Figure S4 (top row). The green bar indicates the estimated optimal direction. (B) The distributions of circular variance of prostriata (light gray) and V1 (dark gray) neurons. Larger value is less selective. (C) Speed tuning curve of a prostriata neuron. The optimal speed for this cell was /s (see Figure S4, second row, for additional examples). The interval between the two vertical green lines is the half-width-half-height bandwidth, which was estimated to be 2.2 octaves. (D) Distribution of the preferred speed of 87 prostriata neurons, measured with moving bars (median = /s). (E) Spatial summation curves of the same neuron shown in (A), illustrating the relationship between neuronal response and bar length (solid lines) or diameter of the dot field (dashed lines). Both the bar and the dot field moved at the speed of 100 /s. The green bars represent bar lengths at which maximal response, as well as half the maximal response, were elicited; see Figure S4 (third row) for other examples. (F) Turning curve of a neuron in response to variations of the density of the kinetic dot fields. The dots were 2 in diameter and moved at 100 /s. The field diameter was kept constant across the tests, being sufficient to cover the entire receptive field of the neuron. Dot density is expressed as the number of dots per steradian (dots/sr), which is equivalent to the number of dots on a circular patch 65.5 in diameter (see also Figure S4, fourth row). In all graphs, error bars represent SEM, arrowheads indicate spontaneous firing rates, and blue curves are best-fit functions. characteristics we observed in prostriata are usually associated with very early stages of the visual system, such as the superior colliculus, the lateral geniculate nucleus, and the granular layer of V1. These include high spontaneous activity, robust and short latency responses to visual stimuli, lack of adaptation to repeated stimulation, lack of selectivity to orientation and direction of motion, and broadband responses to spatial and temporal frequency [24, 25]. However, the receptive fields of neurons in prostriata are comparable in size to, or larger than, those found in high-level visual areas of the inferior temporal and posterior parietal cortex [26, 27]. At the same time, this area shows unique physiological features, such as emphasis in peripheral vision, and receptive fields of constant size across the visual field. Thus, prostriata neurons exhibit few of the defining characteristics of either the dorsal or the ventral streams of visual areas [28, 29], and

6 Current Biology Vol 22 No it is conceivable that this area operates in parallel with these better-characterized information processing pathways. One of the main questions raised by the present results is the origin of the short-latency visual activation of prostriata neurons. One possibility is that these responses derive from cortical areas such as V1 and the middle temporal area, MT [4, 6]. However, given the lack of selectivity of prostriata neurons to spatiotemporal features of the stimulus, this would require an unusual circuit, whereby its receptive fields are generated by nonselective convergence of many neurons with different response properties. Indeed, it is worth entertaining the possibility of an independent subcortical visual pathway to this area, as suggested by previous results in the tree shrew [30]. However, results of retrograde tracer injections in prostriata have never been reported. Prostriata s histological characteristics suggest that it is an evolutionarily ancient area, likely to be shared by most mammals. Whereas visually responsive areas adjacent to peripheral V1 have been described in other species [31 33], their exact homology with prostriata remains uncertain. In cats and flying foxes, lightly myelinated, limbic-type cortices adjoin a much larger proportion of the perimeter of V1 [21, 33]. However, visual responses are not observed throughout this region, suggesting additional areas. In addition, information about physiological response properties is available only for the cat splenial visual area, where neurons differ from those in prostriata by showing sharp orientation selectivities [31]. The present findings are likely to provide a much-needed basis for comparative studies and may prompt noninvasive studies of human brain activity in response to stimulation of peripheral visual fields. Our results demonstrate that cells in prostriata have clearly defined (albeit large) receptive fields and respond well to relatively small, fast-moving objects. This argues against the notion that prostriata cells are simply measuring luminous flux. Features such as the large, uniformly sized receptive fields, emphasis on peripheral representation, and lack of selectivity to spatiotemporal features of the stimulus also seem to exclude a role in high acuity vision. On the other hand, these same features, together with the short-latency activation and widespread connectivity, are compatible with a function in monitoring peripheral visual space for new, unexpected stimuli, and perhaps triggering coordinated defensive responses and shifts in the focus of attention. The observed topographic sampling of the visual field, together with the known connections with areas involved in auditory localization [7, 8] and motor control, particularly of the head and upper limb musculature [2], seem compatible with this idea. Indeed, an interesting possibility suggested by recent studies is that disturbances of a cortical circuit involving prostriata are related to the higher sensitivity to peripheral visual stimulation observed in patients with panic disorder and agoraphobia [34]. Thus, we suggest that prostriata may provide a limbic pathway by which visual information can provide relatively coarse but fast spatial information to command coordinated responses across multiple cortical systems, in situations that demand rapid action. This hypothesis may prove a fruitful guide for future studies exploring its role in behavior and mapping its full network of connections. Experimental Procedures Extracellular recordings were obtained from six anesthetized adult marmoset monkeys. Details of the preparation, visual stimuli, methods of analysis, and histological criteria are given in Supplemental Experimental Procedures. Briefly, tungsten microelectrodes (w1 MU) were directed toward the anterior end of V1 and prostriata. Given the need to explore the far periphery of the visual field, we used panoramic stimuli projected to a hemispherical screen [35]. This method uses a mathematical transformation to project geometrically undistorted stimuli across a wide expanse of visual field, allowing quantitative assessment of receptive field properties (Movie S1). At the end of each experiment, the brains were prepared for histology, and series of sections stained for cell bodies, myelin, and cytochrome oxidase were used to reconstruct the location of every recording site relative to histological boundaries and electrolytic lesions (Figure S1). The experiments were conducted in accordance with the Australian Code of Practice for the Care and Use of Animals for Scientific Purposes. All procedures were approved by the Monash University Animal Ethics Experimentation Committee. Supplemental Information Supplemental Information includes four figures, Supplemental Experimental Procedures, and one movie and can be found with this article online at doi: /j.cub Acknowledgments We thank Katrina Worthy for histological and technical support, Rowan Tweedale for comments on the manuscript, and Janssen-Cilag Pty for the donation of sufentanil citrate. This work was funded by the Australian Research Council (ARC, DP ) and National Health and Medical Research Council (Grant ). The Monash Vision Group is funded by the ARC Special Research Initiative in Bionic Vision and Technology. Received: April 2, 2012 Revised: May 14, 2012 Accepted: May 14, 2012 Published online: June 14, 2012 References 1. Sanides, F. (1972). 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