Functional architecture of the mystacial vibrissae

BEHAVIOURAL BRAIN RESEARCH ELSEVIER

Behavioural Brain Research 84 (1997) 81-97

Research report

Functional architecture of the mystacial vibrissae Michael Brecht a,,, Bruno Preilowski a, Michael M. Merzenich b a Tabingen University, Tabingen, Germany b W.M. Keck Center for Integrative Neuroscience, University of California, San Francisco, USA Received 8 February 1996; revised 10 June 1996; accepted 10 June 1996

Abstract We investigated the transduction operation and function of the mystacial vibrissae, using a comparative morphological analysis and behavioral experiments in rats. Vibrissal architecture was documented in a series of mammals to identify evolutionary conserved features of vibrissal organization. As a result of this analysis, we distinguish between a frontal microvibrissal system and macrovibrissal system of the mystacial pad. The latter was invariably comprised of whiskers aligned in regular rows. In each row, whiskers were oriented perpendicular to the animal's rostrocaudal axis; all shared a specific dorsoventral orientation. In all species, progressing from rostral to caudal in any vibrissal row, there was a precisely exponential increase in whisker length. Each whisker appeared to act as a lever-like transducer, providing information as to whether or not - but not where - an individual vibrissa had been deflected. The rat's frontal microvibrissae system was found to have a vibrissa tip density that was about 40 times higher than that of the mystacial macrovibrissae. In behavioral studies spatial tasks and object recognition tasks were used to investigate (a) search behaviors; (b) single whisker movements; (c) object recognition ability; and (d) effects of selective macro- or microvibrissae removal on task performances. A clear distinction between the functional roles of macro- and microvibrissae was demonstrated in these studies. Mystacial macrovibrissae were critically involved in spatial tasks, but were not essential for object recognition. Microvibrissae were critically involved in object recognition tasks, but were not essential for spatial tasks. A synthesis of these morphological and behavioral data led to the following functional concept: The mystacial macrovibrissae row is a distance decoder. Its function is to derive head centered obstacle/opening contours at the various dorsoventral angles represented by vibrissal rows. This distance detector model is functionally very different from traditional concepts of whisker function, in which the mystacial whiskers were hypothesized to form a fine grain skin-like object-recognizing tactile surface. Keywords: Barrel; Neuroethology; Somatosensory system;Transduction operation of the vibrissa apparatus; Vibrissa function; Vibrissae morphology; Whisker

1. Introduction A comprehension of the basic operations of transduction is crucial for understanding any sensory system. The transduction operations of the vibrissal apparatus have not yet been described in an analytical way. In these comparative morphological and behavioral studies on the vibrissae we ask: H o w are the first order structural features and functional operations of the vibrissal apparatus related? The vibrissae are a m o n g the youngest of the major m a m m a l i a n sensory systems. They are lacking in the m o n o t r e m a t a [22], emerging first in the theria about * Corresponding author. MPI for Brain Research, Postfach 710662, D-60496 Frankfurt/Main, Germany. E-mail: [email protected]

120 million years ago. Facial vibrissae were originally organized into five subfields, and m a n y mammals still exhibit this primitive pattern [ 1,22]. In the vast majority of mammals, the facial vibrissae mystaciales are the most prominent division of the vibrissae apparatus. In this analysis we focus on the function of this orderly array of facial whiskers. For the rat's mystacial vibrissae, it is useful to distinguish between the long, laterally oriented 'macrovibrissae' and the shorter, more numerous and more frontal 'microvibrissae'. Despite a long history of morphological and behavioral work beginning with Vincent (1912) [31] and intense, more recent neurobiological interest beginning with Woolsey and van der Loos (1970) [36], few researchers have attempted to functionally characterize this important sensory system [12]. Moreover, while much research effort has been directed towards studying

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the macrovibrissal physiology at the single whisker level, relatively little attention has been paid to the functional architecture of the vibrissae apparatus or to its operations, considered as a whole. Most commonly, the mystacial macrovibrissae have been described as an extension of the general touch system. The idea that the whiskers operate in a touch-like manner was explicitly stated by Simons 1-27] to apply to the vibrissae mystaciales - the 'macrovibrissae' according to our terminology. This view stressed the functional continuity of neighboring vibrissae, suggested that the vibrissae move in a flexible fluid like way, and hypothesized that they allowed for high resolution perceptions, comparable to those derived from primate finger tips. This general hypothesis has often been expressed with the assumptions that a major function of the whiskers is to expand the search space of the animal[34], and that the whisker array forms a kind of 'long range skin' [27]. Although rarely explicitly stated, many researchers appear to presuppose that the different whiskers of the array are functionally equivalent, and that the whisker array forms a diffuse spatial sensor. In contradistinction to these earlier studies and analyses it is here hypothesized that the mystacial macrovibrissae form a special distance detector sense organ. A description of whisker function has to explain how vibrissal afferents act cooperatively to generate useful information about stimuli for brain analysis. Such a description must be based on the relative functional contributions of the individual whiskers in the mystacial pad. A sense organ by its collective operation accounts for more than any single input element, or the simple sum of input elements [9]. One important prediction of a sense organ concept is that the input elements constituting the vibrissal organ cannot have evolved independently without altering the organ's essential function. If the macrovibrissae comprise a special sense organ, relatively constant whisker arrangements should be seen in many different evolutionary divergent mammals that possess it. Generally, sense organs derive a highly specific and useful stimulus representation. To find out what could be the specific stimulus representation that is derived by the macrovibrissal system, it was first asked: What is the basic architecture of the vibrissae apparatus? Towards that end, conserved species-invariant features of the vibrissae array were defined, in contradistinction to earlier studies, which concentrated on interspecies differences [2,10,17,22,29]. The evolutionarily conserved spatial arrangement of whiskers bears implications for the sampling and coding of spatial information. We investigated this aspect quantitatively and asked: What is coded by a single whisker, as compared with a whisker row or the entire vibrissal array? In the behavioral studies we asked the question: What

roles do different whiskers of the vibrissae apparatus play? Specifically, how does the vibrissal system account for object recognition and for spatial localization? How do the rat's macro- and microvibrissae contribute to these different behaviors? Finally, on the basis of morphological and behavioral data, we present a model of the functional architecture of the vibrissae apparatus.

2. Materials and methods

2.1. Morphological analyses 2.1.1. Animals and species selection Facial vibrissae arrays were studied quantitatively in ten mammalian species, including: Methatheria: Marsupialia: American opossum (Didelphis sp.); Shrew like opossum (Monodelphis domestica); Phalanger (Trichosurus vulpecula). Eutheria: Insectivora: Tenrec (Tenrec ecaudatus); Rodentia (rodents): Albino rat, n = 15, 2-20 months old, males and females, (Rattus norvegicus (Sprague Dawley)); Mouse, n = 8, 10-20 months old, males and females (Mus musculus); Pinnipedia (seals): Common seal (Phoca vitulina); Gray seal (Halichoerus grypus); Sea lion (Zalophus californianus). Primates: Fat-tailed dwarf lemur (Cheirogalens medius). Additionally the vibrissa apparati of cats, ferrets, hamsters and rabbits were studied qualitatively. The rationale of this species selection was based on two premises. First, the rodent and seal species are established 'vibrissae experts' [17,29], and functional features of vibrissal architecture should be particularly pronounced in these species. Other species are distantly related and were selected to identify general, evolutionarily conserved features of vibrissal architecture. The measurements on rodents were performed on freshly killed specimen which came from electrophysiological experiments. Except for the seals, the other measurements were performed on specimen from the animal collection of the Department of Zoology of Tiibingen University (Ttibingen, Germany). These specimen had been preserved in alcohol, which is the preservation method of choice for hair and skin structures. The vibrissae of the pinnipedia were measured from preserved scalps of the animal collection of the Naturkunde Museum in MOnster (Germany). For rats and mice measurements were taken from several specimen, for the other species only single representatives were used; the selection being based on which specimen had the best preserved whiskers. 2.1.2. Definition of macro- vs. microvibrissae and the studied parameters For our quantitative comparison between the rat's macro- and microvibrissae subsystems, we regarded the

M. Brecht et aL /Behavioural Brain Research 84 (1997) 81-97

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and the nomenclature). There are about 30 of these laterally oriented macrovibrissae. The 'microvibrissae' are: (1) The most rostral whiskers

whiskers of rows A, B and the more caudal whiskers of rows C, D, as 'macrovibrissae' (see Fig. 1 for an illustration of the general organization of the rat's vibrissae

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Macrovibrissae-only Fig. 1. Mystacia! macro- and micro~brissae in the rat. (a) Side view of the mystacia] whisker fields. The mystacial microvibrissae-fie]d continues on the inner side of the upper lip. (b) Magnified schematic frontal view of the mystacial microvibfissae. On one side only the skin positions of the follicles of micro- and macrovibrissae are indicated. The lower jaw microvibfissae are not shown. (c) Schematic frontal view of the mystacia! macrovibrissae. On one side only the skin positions and the cauda|most whisker of each row of macrovibdssae as well as the straddlers (dashed) are drawn. Microvibrissae are not shown.

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M. Brechtet al./BehaviouralBrain Research84 (1997) 81-97

of row C, D and E; these are 5-10 whiskers that are oriented and positioned frontally, and thus positioned around the corner from the more laterally directed mystacial macrovibrissae. (2) The 35-60 whiskers of rows F, G, H, I and J (the 15-25 more caudal whiskers of these rows are in organization and length intermediate to macro- and microvibrissae). The 20-35 more rostral whiskers of these rows are typical microvibrissae, a majority of which points downwards (ventrally). For all studied animals, the layout of the vibrissal apparatus, i.e., relative whisker orientation, spacing, position of the vibrissae origins, and vibrissal lengths distribution were defined. After a catalog of speciesinvariant features had been established, additional animals were checked for possible deviations of this scheme. The length distributions of whiskers were measured in all studied mammals. In investigating the length distribution we were interested in the 'functional' or 'effective length' of the whiskers defined as the distance from the skin surface to the vibrissa tip, i.e., maximal distance at which the vibrissa touches an obstacle. In the rodents we simplified this measurement by cutting the whisker just above the skin. Regression analysis was used to evaluate the relationship between functional whisker length and position. We also estimated whisker density for quantitative comparisons between the rat's lateral macrovibrissal and frontal microvibrissal subsystems. In the vibrissat system, the distance between neighboring whiskers is a morphological indicator of the spatial sampling density. Whisker density equals the number of whiskers per unit area within the sensory plane that they form. The most appropriate and simplest definition of the sensory plane formed by the vibrissae is the plane formed by the vibrissae tips. This plane was approximated as a set of four trapezoid shapes formed by the whisker tips of the five whisker rows (the straddlers were assumed to be standing in line with the rest of the row). 2.2. Behavioral analyses 2.2.1. Animals Studies were performed in four adult, blind, female RCS-rats (1-2 years old, 150-250g weight), with an inherited retinal defect, and in five adult male albino rats (5-6 months old, 200-300g weight, SpragueDawley, Interfauna Tuttlingen). In their home cages, the animals had access to water and food ad libitum throughout the study and the experiments. Room lights were on a regular 12-h light/12-h dark schedule. 2.2.2. Recording of whisker movements During the object discrimination paradigm described below, the movements of single whiskers were recorded by means of a special recording technique: Single whiskers of the rat were marked with a miniature patch reflex

foil. Measurements taken of whiskers with and without foil indicated that this foil patch did not affect whisker movements. A light source was placed laterally and its light reflected onto the scene by a 45 ° inclined halfsilvered mirror. The video recordings were made from above through the mirror. The light gain could be maximized by adjusting the focal length of the camera to match the virtual position of the light source in the mirror. An RCA-camera with a sampling rate of 50 Hz was used to record movement sequences. The shutter of the RCA-camera was open for the complete frame duration (20 ms), and the movement of the labelled vibrissal spot during this time appeared as a variable length white line in the frame. Some sessions were taped in darkness using infrared light. 2.2.3. Object discrimination task: Psychophysics of object recognition Search time measurements for the identification of a target object in the presence of a number of distractor objects have been a major paradigm for studying visual object recognition in humans [30,18]. This task was adapted to study vibrissal object recognition in albino and blind rats. Rats were presented with cookies of different sizes and shapes that tasted sweet or bitter depending on size or shape. Small cookies were made from a batter that contained sugar, butter and flour (1:2:6), and a few drops of water. Non-target cookies were embittered with caffeine, which is odorless. Cookies were flat ( 1-2.5 mm thick) geometric forms. Rats had to discriminate between sweet small right triangles (6 mm side length) as targets and bitter small squares ( 6 m m side length) and/or bitter large triangles (8 mm side length) as distractors. Catch trials were run with well trained rats; in such trials embittered target-shape cookies or sweet, nonembittered distractor-shape cookies were presented to each animal (5-8 such tests per animal). Several sessions of the albino animals (including catch trials) were performed under infrared illumination or in total darkness. The rats were trained to perform the discrimination, with the discriminanda presented on an elevated stage (see Fig. 4a). Two types of experiments were performed. In the first, animals were presented with one or no targets (a sweet small triangle) together with a variable number of distractor cookies. This arrangement was designed to determine the interdependence of object number and search time. In a second experiment the target cookie (a small sweet triangle) was presented to the rats together with 15 distractor cookies (small squares) in a regular 4 x 4 array. This test situation is shown in Fig. 4a. The target appeared at random positions in the array on different trials. In between, trials were run in which single targets or distractors without additional distractors were presented at random positions of the array. An objective of

M. Brechtet al./BehaviouralBrainResearch84 (1997) 81-97 this experiment was to determine the relationships between target positions and search times. These tasks were also used to assess the rat's object recognition abilities, using search time measurements before and after whisker removal. All trials were videotaped. Search time was determined in frame by frame analyses. 2.2.4. Spatial task The locating of a single edible cookie in a 75 × 80 cm field was chosen as a spatial task for the four blind RCS-rats. Two metal cylinders (10 cm diameter and a platform (20 × 20 x 7 cm) that appeared at random locations in the open field served to enhance the spatial complexity of the cookie locating task. The cookie was randomly positioned in this field. 2.2.5. Selective whisker removal In the four blind animals, facial vibrissae were removed in two steps involving the two facial whisker subdivisions of mystacial macrovibrissae and microvibrissae. Before and after each removal, rats were tested on object recognition and spatial (cookie locating) task. Trials were analyzed for search time, as well as for hits and misses. A trial was scored a 'hit' if the animal picked up the target cookie during the first search attempt. A trial was scored as a 'miss' if the rat turned its head away from the cookies, stopped head movements and ended the search. For whisker removal, animals were held in a plastic bag with a snout opening. Pseudo-shaving control procedures in which the animals were handled in the same way as for whisker removal were interspersed with actual removals. For these control procedures, animals were immobilized in the bag for several minutes, and the skin was palpated with a pair of scissors or a shaver, as in the removal procedures. In two animals, the mystacial macrovibrissae were removed first with a pair of scissors, with the external microvibrissae (mystacial and lower jaw) trimmed second, using an electric shaver. In the other two animals, the vibrissal removal sequence was reversed. All test trials within the whisker removal experiment were run within 5-6 days, with 35 object recognition tasks and 50 cookie location tasks/animal/condition (Pretest, pseudo shaving, microvibrissae or macrovibrissae removal, micro- + macrovibrissae removal).

3. Results

3.1. Morphology of the vibrissal system 3.1.1. The dist&ction between lateral macrovibrissae and frontal microvibrissae In the course of a simple analysis of vibrissae arrays, it became clear that the longer, more lateral mystacial

85

vibrissae and the shorter, more frontal mystacial vibrissae have different functional characteristics. Since it was also found that whisker length was a key parameter in the vibrissal system, it appeared appropriate to classify whiskers with respect to their sizes. The macrovibrissae are the long, more posterior, 'classic' mystacial whiskers; the microvibrissae are the shorter, more anterior whiskers. ~ For macrovibrissae, whisker length was a major parameter determined by the position of the whisker tip relative to the surrounding whisker tips and the geometry of the sensory plane formed by the whisker tips. For the microvibrissae, whisker length was only a secondary parameter with respect to the relative position of the whisker tip. The transition between macro- and microvibrissae is not abrupt. Nevertheless, the following results justify distinguishing them. There are 40-70 microvibrissae (see also Fig. 1). The quantitative morphology of microvibrissae is complicated by the short length of these whiskers and the difficulty of differentiating them from fur hair. Moreover, unlike macrovibrissae, missing microvibrissae are not easily detected. The rat has two further microvibrissal fields not included in our mystacial macro-/microvibrissae comparison. One internal microvibrissae field is on the inner side of the upper lip; this field in the rat's mouth is continuous with the above-described external field and consists of 20-40 whiskers in a high-density arrangement. Another microvibrissae field is found on the rostral aspect of the lower jaw (ca. 30 whiskers). As documented in Table 1 the organization of the rat's mystacial macrovibrissae and the external microvibrissae is quite different. Table 2 tabulates some of the quantitative differences between mystacial macro- and microvibrissae. The most obvious differences are found in the length of the whiskers and the density of the sampling array. The latter is >40 to > 100 times higher for of the microvibrissal system than for the macrovibrissal system. 3.1.2. Species-invariant architecture of the mystacial macrovibrissae Qualitative invariances of the mystacial macrovibrissae. In many mammals, including all species studied here, the mystacial whiskers or macrovibrissae are the most prominent or the only vibrissae division [10,22]. In a majority of mammals, they consist of a set of whiskers that are highly ordered with respect to their location, lengths and orientations. A central observation is that rows are the basic units of the mystacial pad: (a) Rows are found in all species. (b) Rows are always straight and approximately parallel.

1We thank H.U. Schnitzlerfor suggestingthis terminology.

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M. Brecht et al./Behavioural Brain Research 84 (1997) 81-97

Table 1 Qualitative comparison between the macrovibrissae the microvibrissae

Morphological characteristics

Single whisker Mystacial array

Morphological location

Major field Other occurrences

Movement

Whisking movement Head movements

Table 2 Quantitative comparison between the microvibrissae

Macro-vibrissae

Micro-vibrissae

Lateral orientation (on the average) Sensory plane almost perpendicular to skin and rostrocaudal axis A-, B- row and the non frontal parts of C-, D-, and E-row Many additional subfields with few or single whiskers Major role in target contact Minor role in target contact

Diverse orientations (ventral and frontal are most common) Sensory plane more parallel to skin

macrovibrissae and

Macrovibrissae

Microvibrissae

Length Number

> 4 mm 30-35 (mystacial)

Estimated extent of the sensory plane Average whisker density Minimum whisker density Maximum whisker density

16.4 cm2(10-25 cm2)

< 7 mm 40-70(external, mystacial) 0.69cm2(0.3-1.5 cmz)

2/cm 2

87/cm 2

0.35/cm2

10/cmz

25/cm2(10-50/cm2)

281/cm2(200-600/cm2)

Note. Our observations relate to the mystacial macro- and microvibris-

sae division and not to other vibrissae subfields. The term sensory plane refers to the plane formed by the vibrissae tips. The quantitative measurements on number and sensory plane refer to one side of the head only.

(c) Whiskers in a row are close together, often only a minimal positional distance is observed. (d) There is a relatively great distance between neighboring whisker rows; often a m a x i m u m distance spacing of rows is seen. (e) The whiskers within a row share one dorsoventral orientation, which is maintained during whisking movements. (f) Whiskers of a row sample highly overlapping spatial information. As m a n y as nine organizational constraints have been found to be invariant in the 14 species studied. These organizational principles of the mystacial macrovibrissae are summarized in Fig. 2. There is a strict whisker-specific multiparametric order in the array. Thus, with knowledge of the relative location of a whisker, its relative spatial orientation and its relative length are predictable. According to their orientation and bending, the whiskers point away from each other, i.e., they diverge. It is important to note that the vibrissae do not form a cloud-like distribution in space. Moreover, vibrissae origins do not follow an

The most frontal parts of C-, D-, E- row and F-, G-, H-, I-, J-row Only two other subfields on the lower jaw and inside the mouth. No single or few whisker subfields Unknown Major role in target contact

equidistant (maximum spacing) distribution on the pad. Rows very strictly confine locations and specific dorsoventral orientations of their whiskers. The positions of vibrissae origins are generally crowded towards the front of the animal. However, in all examined species, the macrovibrissae were oriented laterally, and thus do not form a forerunning sensory array. Quantitative invariant length tuning - organ-pipe row architecture. In all studied species, effective whisker

length was found to increase exponentially along rows, proceeding in the rostral-to-caudal direction. Whisker length was plotted against whisker position on a logarithmic scale in Fig. 3a for the A-row, and in Fig. 3b for the D-row. These straight line functions reveal an exponential effective whisker length versus position scale. The effective length of the next more caudal row neighbor of any whisker was 1.2 to 1.6 times longer, a constant value depending on the species and the specific row. The intraspecies variance of whisker length tuning along the row was examined more closely in rats and mice. As shown in Fig. 3c and 3d the same pattern as in inter-specific comparisons was obtained. While the absolute whisker lengths differed between individual rats and mice, the relative whisker lengths (the exponential lengths versus positions distribution) applied to all examined individuals. Another observation from the rat and mouse data concerns the so-called 'straddlers'. The straddlers are the four caudal-most whiskers of the mystacial pad, and are found only in rodents. They are laterally displaced relative to the whisker rows. The straddlers deviated (towards shorter lengths) from an exponential lengths versus positions scaling. Finally, regression analyses were used to evaluate how well an exponential function described the relationship between whisker position and length. For the D-row whisker-position relationship, an exponential function explained most of the variance; for the D-row of the various examined species the correlation coefficients between exponential fits and data were between

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Whisker position constraints: 1. A majority of the animal's macrovibrissae are located on the mystacial pad: otherwise random positions.

2. Whiskers are organized in rows. 3. Rostrocaudal parallel rows.

Whisker orientation constraints: 4. Maximal spacing between rows. 7. Whisker orientation perpendicular to rostrocaudal 5. Minimal spacing of neighboring axis. whiskers within the row.

Whisker length constraints: 6. Maximally rostral position of the 8. Divergence of whisker vectors within the dorsoventral plane whisker row. of the row.

9. Exponential length tuning along the whisker row.

Fig. 2. Principles of mystacial pad architecture. The first column describes constraints on position of the whisker origin. Starting from the top, the rules which lead to a species-invariant distribution of whisker positions (bottom) are listed and illustrated. The second column describes constraints on whisker orientation given the species invariant whisker positions. The third column illustrates the rule which leads to the species-invariant distribution of whisker lengths. All species studied showed the vibrissae organization illustrated on the bottom right.

r2=0.942 and 0.994 (species average r2=0.978). Similarly, high correlation coefficients between exponential fits and length position data were observed in intraspecific comparisons for the D-Row of rats (range: r2=91.6-100, average r2=96.8) and mice (range: r2=92.2-98.7, average r2=96.9). The excellent fit between effective whisker length and sensory surface position by an exponential function is shown in Fig. 3e. For the average laboratory rat, the deviation from the

predicted exponential lengths was less than 2 mm per whisker. Many specimens showed deviations of less than 1 mm per whisker from an exponential length scaling. All other species studied showed an equivalently precise length versus position relationship. While the effective length distributions along rows were species invariant, the length distributions along the arc (i.e., over columns) of the mystacial pad did not follow any strict species invariant rule (Fig. 3f).

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M. Brecht et aL /Behavioural Brain Research 84 (1997) 81-97

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M. Brecht et al./Behavioural Brain Research 84 (1997) 81-97

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3.2. Behavioral observations on vibrissal perception in the rat 3.2.1. Object recognition Albino- and blind RCS-rats achieved high levels of performance in cookie shape and size discrimination

tasks. Task acquisition was fast (within a day or two), and errors as measured by false positives (when nontarget cookies are picked up) were few (1% or less). The results from the catch trials with both albinos and blind animals indicated that the animals discriminated the cookies primarily or exclusively by shape:

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M. Brechtet al./BehaviouralBrainResearch84 (1997) 81-97

More than 90% of the embittered target-shapes (19 of 21 such cookies) were taken up by the animals, and less than % 5 of the non-embittered distractor-shapes (3 of 70 such cookies) were taken up by the animals. Albinos performed the discrimination in darkness in a shape dependent manner (normal trials as well as catch trials). Thus both blind animals and albinos appeared to be able to use tactile cues for the discrimination. Search behavior. Some species such as rats and hamsters whisk, that is, they move their whiskers in rapid back-forth successions, generally within the plane of a macrovibrissae row [4, 33, 34]. When blind rats or albino rats searched an area for cookies they whisked intensely. If small object numbers had to be discriminated the behavioral strategies of albino rats and blind animals were very similar. It was often seen that a rat passing in the vicinity of the cookies detected them with its long macrovibrissae. After detection, a specific sequence of behaviors followed. Invariably, the rat turned its head towards the cookies. During a discrimination phase that varied in length as a function of the number of cookies to be discriminated (0.2-5 s), the rat oriented frontally toward the cookies and ultimately stationed its head directly over the target cookie. At that time, the microvibrissae between nose and mouth were in direct contact with the target cookie. The retrieval of the target cookie followed. Role of identified whiskers in the task. Videotaped movements of single mystacial macrovibrissae during the object discrimination task showed that these whiskers maintained a perpendicular orientation with regard to the animal's rostrocaudal axis throughout the task. The whiskers of the C-row had a lateral orientation, the A-row a more dorsal orientation and the E-row a more ventral orientation. The caudal macrovibrissae deviated slightly backwards from the average lateral orientation, and the anterior mystacial whiskers had a more frontal orientation. In the context of the search behavior, this lateral orientation implies that the macrovibrissae contact the target cookie during search, before the animals turns toward the cookies, i.e., before the beginning of the discrimination. The long mystacial macrovibrissae were not in contact with the cookies during the discrimination phase. This pattern of whisking movements and target approach with a centering of the microvibrissae relative to the discriminanda was very similar or indistinguishable between blind animals and albinos. Quantitative aspects of vibrissal search. Blind rats investigated a cookie cluster by moving their heads from one cookie to another. This one-by-one inspection strategy was also indicated by the quantitative analysis of the dependence between search time and object number. A linear increase in search time with display size was recorded. This increase in search time was twice as steep in the target-absent condition as in the target-present condition. These observations demonstrate that vibrissal

search occurs as a serial, self-terminating process. This conclusion applies only to blind animals. In one of the recognition tasks the four blind rats were presented with an ordered 4 x 4 array of cookies (see Fig. 4a); the side length of the array was 3.2 cm, and therefore considerably smaller than the maximum diameter of the whisker fan (which is about 11 cm). In all animals, there was a great increase in search time from the frontal row of the array to the posterior rows of the cookie display (Fig. 4b). Moreover, on average, targets in middle positions of the rows were found faster. When single targets or distractors without the distractor objects were presented at random positions of the array the search times were very short (shorter than the average search time in the first row) and largely uniform cross the array positions. This indicates that the search time increase across array positions in our paradigm is due to the perceptual load induced by our distractor objects. All of these observations are consistent with the conclusion that the animals searched the display serially, starting from the middle position of the first row and moving on to the side and the posterior rows. Effects of selective whisker removal. Figs. 5 and 6 illustrate the effects of selective whisker removal in the genetically blind RCS-rats on object recognition and the spatial cookie search task in the open field. Macrovibrissae removal did not result in a significant search deficit in the object recognition task (Fig. 5), but led to a dramatic search time increase in the spatial cookie location task (Fig. 6). On the other hand, microvibrissae removal had no visible effect on the cookie locating task (Fig. 6), but resulted in a profound deficit in object recognition ability (Fig. 5). Thus, in these trained RCS-rats, a double dissociation between microvibrissae accounting for object recognition and macrovibrissae accounting for spatial object detection was recorded.

4. Discussion From these results, three interconnected hypotheses are derived. (1) The long mystacial macrovibrissae and the short frontally directed microvibrissae comprise two functional subdivisions of the rat's vibrissal system. (2) The microvibrissae can be viewed as an object recognizing sense organ. They provide the sampling density that is crucial for tactile object recognition. They play a negligible role in sampling spatial information. (3) In contrast, the mystacial macrovibrissae can be viewed as a distance detecting/object locating sense organ. They have an evolutionarily highly conserved architecture. We suggest that they function as a

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4.1. The distinction of a fovea-like microvibrissae system and a spatial macrovibrissae system Our object discrimination experiment and control procedures - namely the use of blind animals, task performance of albino animals in darkness, catch trials,

and the selective whisker removal - show that both albinos and blind animals are capable of tactile object discrimination. Our video recordings indicate that both groups appear to use a similar behavioral strategy. The behavioral data point to a different role for macroversus microvibrissae in an object recognition task. This difference is manifested (a) by the rat's search behavior; (b) by the observation of whisker movements; and (c) by behavioral changes - or lack of changes - following

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94

M. Brecht et al./Behavioural Brain Research 84 (1997) 81-97

selective macrovibrissae removal. At least in blind rats the mystacial macrovibrissae play only a limited role and are not sufficient by themselves - for object recognition. The findings from the vibrissal search experiments, the object array experiment and the rat's search behavior indicate that the animals searched the object displays serially. The large search time differences across the positions of the object display indicate that the rat is not able to 'view' the entire array at once on a level adequate for object recognition, but had only a small effective tactile window for sampling objects, smaller than the 3.2 × 3.2 cm of the display, and far smaller than the sensory plane of the macrovibrissae (> 30 cm2). From our removal results we argue that object recognition occurs primarily in a relatively small tactile window corresponding to the microvibrissae. This general distinction between the functional roles of vibrissal subsystems is supported by observations on the morphological differences between macro- and microvibrissae. Whisker density in the microvibrissae system is about 40-100 times higher than for the macrovibrissae system. Based on receptor density, one might think of the microvibrissae as a fovea-like system, brought into action after stimuli to be explored are first located by the macrovibrissae. Behaviorally both albinos and blind animals appear use a kind of 'foveation' strategy which brings the microvibrissae onto the discriminanda. Two studies on vibrissal object recognition, one on the walrus by Kastelein and van Gaalen 1-16] and one on the sea lion by Dehnhardt I-5] report qualitatively similar findings. According to these studies, neither of these pinnipeds use their long more caudal whiskers for object recognition, but engage their short frontal vibrissae for such tasks. Our behavioral observations and the macrovibrissae removal experiments demonstrate a major role of the macrovibrissae in spatial, object-locating tasks. This role has been recognized since the first behavioral study on whiskers by Vincent [31], who described deficits of dewhiskered rats on maze tasks. A long list of related observation has been published (e.g. 1-23,24]). A particularly interesting effect results from one-sided vibrissae removal (hemi-vibrissotomy), which causes the animal to move along a wall with the vibrissae-intact body side facing the wall 1-20].

4.2. Functional architecture of the macrovibrissae: Distance detector theory 4.2.1. Distance detector theory: Computational tasks of the mystacial macrovibrissae How does the macrovibrissae architecture function in sampling spatial information? Straight, generally densely spaced whisker rows appear to be fundamental units of the macrovibrissal

pad. The macrovibrissae are not arranged for a homogenous, equidistant sampling of space. As the rows confine whisker positions and orientations, whiskers of a row occupy - and are whisked through - overlapping segments of space. What is different about the whiskers of a row is their length. Indeed, whisker length varies highly systematically along the rows (and not along arcs, i.e., columns) in all studied species. From these facts it is concluded the whisker row is a distance decoder comprised of binary distance detectors; the longest (the most caudal) untouched whisker codes the minimal distance to an obstacle. The corresponding computational task of the mystacial pad is to derive obstacle/opening contours, the dorsoventral angles of which are coded by the rows in a sensory plane at the top of the animal perpendicular to its rostrocaudal axis. This distance contour information is generated in a robust binary form, and coded in head-centered coordinates. Fig. 7 schematically displays the properties of such a hypothesized distance detector array. The idea that the row performs an orderly extraction of distance information provides a functional explanation for the fact that the mystacial pad is made from row-modules with their organ-pipe architecture. The observed precision of effective whisker length tuning is quite extraordinary if one considers the permanent random mechanical degradation (breakage, wear, bending) of the vibrissae due to their exposed body position. This precise exponential length tuning is requisite, if the row is providing a fine scale for distance, and is the basis for breakdown of spatial information into a coordi-

Fig. 7. Hypothetical transduction operation of the macrovibrissae according to the distance detector theory. The sensory plane is oriented perpendicularly to the animal's rostrocaudal axis and different rows of the mystacial macrovibrissae code for different angles. A single row functions as a distance decoder, composed of a set of whiskers of different length, each acting as binarily (touched/untouched) coding distance detector. Short distances are over-represented. An obstacle (gray bar) deflects all whiskers (black) longer than the minimal obstacle distance. The system defines contours between longer touched whiskers and shorter untouched whiskers. Moreover, the sign of the contour is fixed: Only contours of obstacles (outside) and openings (inner side) can be detected.

M. Brecht et al./Behavioural Brain Research 84 (1997) 81-97

nate system formed by labeled lines. Moreover, it is a scaling scheme that overly represents the short and presumably more important distances and might optimize the sensory contribution of each distance detector (whisker) by keeping the relative length difference between neighboring whiskers constant. While whisker origins are closely spaced, there is some divergence of the whiskers of a row. This might be due to the need of reducing mechanical crosstalk between neighboring whiskers. The lateral orientation of the mystacial whiskers maximizes the search space for distance information. The lateral orientation and the minimal rostrocaudal extent of the pad indicates that the rostrocaudal dimension is secondary and that the functional sensory plane formed by whisker tips is oriented laterally, perpendicular to the rostrocaudal axis of the animal. According to this view, the rostrocaudal whisking movement might be considered a distance scanning behavior, as it allows a row of whiskers - all of different length - to move through an overlapping segment of space. While we suggest that the set of different length whiskers of a row provides an efficient mechanism for distance estimation, distance information is not easily available from single whiskers. The vibrissa hair itself is a dead structure, and the deflections sensed by the receptors around the whisker shaft [3,21] reveal no direct non-ambiguous information about the length (= distance) at which the whisker is deflected. The functional properties of a distance detector array might be outlined by contrasting them with an alternative view of mystacial whisker function, which postulates a skin-like operational mode of the mystacial array [27]. In a 'skin-model' the vibrissae tips are hypothesized to form a sensory array comparable to a fingertip. Table 3 lists tentative differences of these models. A distance detector array seems to be suited to provide coarsely coded spatial information for orientation and object detection, as opposed to high-resolution information for object recognition, which a skin-like sensory array is more suited for. In a distance detector array the

95

stimulation of a shorter whisker automatically implies that the longer whiskers are stimulated as well. Therefore, the type of transduced information represents obstacle/opening contours between sets of engaged (longer) and non-engaged (shorter) whiskers, as compared to pixel-like images of surfaces sensed by the skin. Additionally, the sensory surface of a distance detector array is anisotropic, because the sign of the contour is not interchangeable. The obstacle is always outside, and the opening is always inside. This differs from the isotropic surface of a skin-like array. A distance detector array forms a discontinuous sensory surface with perpendicularly oriented whiskers and a rigid vibrissa apparatus. The sensory surface of a skin-like array is more continuous, with flexible whisker orientations in a fluidlike vibrissae apparatus [4]. Thus, the coding of spatial information in both models is grossly different. We argue that the architecture of the macrovibrissae supports best detector functions, but this does not imply that binary coded obstacle/opening contours are the only information available from the macrovibrissae. The single whisker can provide more elaborate inputs, such as successive deflection (timing = surface roughness) and deflection-directional information. At the same time our behavioral results do not support the idea that this single whisker information is generally used to deduce the fine geometry of a contacted obstacle. Like other sense organs the macrovibrissae certainly serve different and multiple functions depending on species and behavioral context. Thus, while the distance detector model tries to capture what we consider to be basic principles of macrovibrissae operation, it cannot constitute an universal or exclusive theory of the macrovibrissae.

4.2.2. Morphological and behavioral evidence As demonstrated by the way that the distance detector model was derived, a distance detector array hypothesis requires and explains the morphological invariances of the mystacial pad. At the same time, several of these

Table 3 Functional comparison between the distance detector model and a skin-like mode of operation of the macrovibrissae

Behavioral function Type of transduced information Properties of the sensory surface

Spatial coding

Distance detector array

Skin-like array [27]

spatial orientation and monitoring obstacle/opening contours functionally non-continuous anisotropic perpendicular orientation necessarily rigid maximal distance information minimal rostrocaudal information representation in spatially fixed head-centered coordinates binary, coarse, touched/untouched coding across the input array

object recognition and spatial orientation pixel-like image of surfaces functionally continuous isotropic flexible orientation fluid, mosaic-like minimal distance information rostrocaudal information preserved flexible spatial relationships fine coding of relationships and patterns across the input array

96

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morphological features appear to be inconsistent with a skin-like operation of the macrovibrissae. Thus: (1) The spatial resolution of the long mystacial whiskers is limited, because of the low number of only 30 whiskers which erect a huge whisker fan. (2) The neighborhood relationships of vibrissae tips (the major information communicated by a skin-like array) play only a secondary role in the mystacial pad. The vibrissae lengths are different. The peripheral whisker rows are generally shorter than the central whisker rows, and the vibrissa tips are therefore not lying in a plane. The rotatory whisking movements distort the proportional relationships of the whisker tips. (3) The mystacial whiskers are oriented laterally and not frontally. Experimental results not fully consistent with our hypothesis are recorded in reports on extremely fine texture discriminations of two grids by the mystacial macrovibrissae [4,11]. However, while these studies provide evidence for vibrissal texture discrimination, both studies were not designed to differentially test the involvement of macro- and microvibrissae in this task. Therefore, at present it can not be judged how macroand microvibrissae compare in their texture discrimination abilities and which whiskers the rats preferentially use under such circumstance. The distance detector theory might be tested by its behavioral predictions. We predict that animals are massively superior in estimating distances rather than extents with their vibrissal system. In a Y-maze forced choice paradigm in which the rats have to chose either the wider of two gates or have to select the wider of two walls, the animals are expected to perform substantially better in the gate-choice-task. Similarly, we predict that the distance-estimation-abilities of the animals should quantitatively covary with the vibrissal architecture. This could be tested in the gate-choice paradigm with an animal whose whiskers have been clipped except for the C-row. If the maximal distance which the longest whiskers can touch is taken as a reference and progressively smaller distances are to be discriminated by the animal, an abrupt increase in the animal's distance-estimationability (measured by error rate or reaction time) should be seen when the distance becomes small enough for the next shorter whisker to touch. Such a 'quantal' course of the discrimination curve would also demonstrate the detector nature of the whisker signal. 4.2.3. Distance detector theory and existing neurobiological data o f the vibrissal system How does a distance detector theory fit into the rich data on the neurobiology of the barrel cortex? (1) While more recent electrophysiological and imaging studies demonstrate multiwhisker RFs, there is a

(2)

(3)

(4)

(5)

consensus that strong response preferences for single whiskers are a major characteristic of barrel cortex neurons [14,25,26,28,32]. Together with the fact that multi-whisker stimulation almost invariably leads to inter-whisker inhibition, we conclude that a binary touched/untouched signal is the major information format in the barrel cortex, as opposed to selectivity for complex multi-whisker stimulation patterns. There is an unexplained anisotropy of inhibitory interaction in barrel cortex [19]. Stimulation of caudal vibrissae inhibits responses to stimulation of more rostral vibrissae more strongly than rostral stimulation inhibits responses to caudal whiskers. The stronger inhibition from long to short whiskers selectively enforces obstacle (outside)/opening (inside) contours, and thus, this anisotropy appropriately relates to the anisotropy of the mystacial pad according to a distance detector theory. Lesions in the barrel cortex do not lead to a significant change in the behaviorally measured temporal or behavioral detection thresholds for macrovibrissa deflection. On the other hand, lesions to the appropriate barrels impair the rat's ability to use the macrovibrissa for estimating distance in a gap jumping task [ 13]. These results are expected if the barrel cortex does not generally extract high resolved temporal and deflection information from macrovibrissae inputs but is concerned with extracting spatial distance information from macrovibrissa inputs. In rat and mouse macrovibrissae barrel cortex physiological [25,28] and anatomical evidence has accumulated for a preferential connectivity between the barrels of a row, as compared to the connectivity of barrels between neighboring rows. This type of connectivity is consistent with the claim that the rows are functional units of the macrovibrissae array. The tectal representation of the vibrissae has been studied in the mouse [6-8] and more recently in the rat [ 15]. In these neural representations, macrovibrissae are strongly emphasized in areal extent and are aligned with the overlaying map of the visual field. The mapping of vibrissal space onto visual space matches the layout of a distance detector system (a caudal to rostral coding of eccentricity, with the rows coding for different angles). The existence of a precise, very reproducible mapping of macrovibrissae inputs onto visual space is strongly consistent with the idea that the macrovibrissae code distance in fixed, head-centered coordinates.

4.3. Conclusion

From morphological and behavioral observations, it is hypothesized that the mystacial macrovibrissae organ

M. Brecht et al./Behavioural Brain Research 84 (1997) 81-97

functions as distance detector array that derives distance contours. This concept is very different from traditional touch-like views of macrovibrissae function. In contrast to the macrovibrissae, the microvibrissae appear to form a high resolution tactile sensor and operate in a more touch-like manner. It is obvious, that the operational mode of the vibrissal array cannot be resolved by a single study, and we do not claim that our data definitely prove the distance detector theory. We also realize that some may consider our theoretical conclusions to go beyond the presently existing data. This, however, we think is acceptable, because it provides a frame for further studies to differentially test the competing models of whisker function.

[ 11 ]

[12]

[13]

[14] [15]

[16]

[ 17]

Acknowledgement We like to thank Manfred Ade, Dean Buonomano, Dan Goldreich, Josh Gordon, Renate Ruhl, Professor Schnitzler and the Naturkunde Museum MOnster. The RCS animals were kindly provided by Professor LaVail's laboratory. Bruno Preilowski was supported by a Fellowship of the McDonnell-Pew Trusts.

[18] [19] [20]

[21] [22] [23]

References [24] [ 1]Ade, M., Diplomarbeit, Fakult~it for Biologie der Universit~t Tiibingen, 1993. [2] Ahl, A.S., Relationship of vibrissal length and habits in the sciuridae, J. Mammal., 68 (1987) 848-853. [3] Andres, K.H., Ober die Feinstruktur der Rezeptoren an Sinneshaaren, Z. Zellforsch., 75 (1966) 339-365. [4] Carvell, G.E. and Simons, J.D., Biometric analysis of vibrissal tactile discrimination in the rat, J. Neurosci., 10 (1990) 2638-2648. [5] Dehnhardt, G., Preliminary results from psychophysical studies on the tactile sensitivity in marine mammals. In J. Thomas and R. Kastelein (Eds.), Sensory Abilities of Cetaceans, Plenum Press, New York, 1990, pp. 435-446. [6] Dr~ger, U.C. and Hubel, D.H., Physiology of visual cells in mouse superior colliculus and correlation with somatosensory and auditory input, Nature, 253 (1975) 203-204. [7] Dr~iger, U.C. and Hubel, D.H., Responses to visual stimulation and relationship between visual, auditory and somatosensory inputs in mouse superior colliculus. J. Neurophysiol., 38 (1975) 690 713. [8] Drager, U.C. and Hubel, D.H., Topography of visual somatosensory projection in mouse superior colliculus, J. Neurophysiol., 39 (1976) 91-101. [9] Gibson, J.J., The Senses Considered as Perceptual Systems. Houghton Mifflin Company, Boston, 1966. [ I0] Goldschmid-Lange, U., Ober die morphologischen Unterschiede

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