Finding your way in the dark: the retrosplenial cortex contributes to spatial memory and navigation without visual cues

Path integration is presumed to rely on self-motion cues to identify locations in space and is subject to cumulative error. The authors tested the hypothesis that rats use memory to reduce such errors and that the retrosplenial cortex contributes to this process. Rats were trained for 1 week to hoard food in an arena after beginning a trial from a fixed starting location; probe trials were then conducted in which they began a trial from a novel place in light or darkness. After control injections, rats searched around the training location, showing normal spatial memory. Inactivation of the retrosplenial cortex disrupted this search preference. To assess accuracy during navigation, rats were then trained to perform multiple trials daily, with a fixed or a different starting location in light or darkness. Retrosplenial cortex inactivation impaired accuracy in darkness. The retrosplenial cortex may provide mnemonic information, which decreases errors when navigating in the dark.     

Olfactory cues and accessory olfactory bulb lesion: effects on sexual behavior in the cyclic female rat

The influence of olfactory cues and accessory olfactory bulb (AOB) lesion on female sexual behavior was studied in virgin female Wistar rats. In Experiment 1, it appeared that distance or contact exposure to male urine soiled bedding for 8 hours before testing increased sexual receptivity, i.e., the number of receptive females at 18:00-19:00 on proestrus. In Experiment 2, we observed that sexual receptivity at 18:00-19:00 on proestrus was not affected by AOB lesion as compared to sham-operated females. In Experiment 3 the effects of both AOB lesion and olfactory cues were analyzed. Sexual receptivity at 18:00-19:00 on proestrus did not significantly differ in sham-operated and accessory olfactory bulbectomized females both exposed to the odor of male urine. Regarding lordosis quotient in the three experiments, no significant difference was observed. Mechanisms whereby olfactory cues and/or AOB lesion modified female sexual behavior on proestrus in virgin female rats were discussed in the light of previous and present observations.     

Use of proximal and distal cues in place navigation by mice changes during ontogeny

The ontogeny of the ability of C57BL/6 mice to use different cues for spatial learning was examined in several Morris water maze tasks. In the first two studies, three learning procedures were used, in which only distal cues (place learning), only proximal cues (cue learning), or both proximal and distal cues (cue + place learning) were pertinent to localize the platform. The results indicated that whatever the procedure, 22-day-old mice showed the same capabilities as adults. Moreover, in the cue + place-learning procedure, although the distal cues were not necessary to solve the task, both young and adult mice demonstrated the integration of distal information by exhibiting a strong spatial bias during a probe test. However, in the third experiment, it was shown that nonpertinent proximal cues perturbed 22-day-old mice in a place-learning procedure. Taken together, these results suggest that while even the youngest mice show striking spatial navigation abilities, young mice give greater importance to proximal cues for orientation whereas adults preferentially use distal information. © 1996 John Wiley & Sons, Inc.     

The effect of familiar visual and olfactory cues on the aggressive behavior of mice

Adult male mice, isolated for 14 days, were tested for aggressiveness against standard castrate opponents under five conditions: (1) the home cage; (2) visual cage (visual characteristics similar to the home cage); (3) olfactory + visual cage (olfactory and visual characteristics similar to the home cage); (4) olfactory cage (a completely strange cage with olfactory characteristics similar to the home cage); and (5) strange cage (a completely strange cage). The results show a significant increase in aggressive behaviour with progressively more familiar environments. It is also shown that familiar olfactory cues have a greater enhancing effect on aggression than do familiar visual cues. The results are explained in terms of the conflict between attack and competing behaviours.     

Olfactory cues and pig agonistic behavior: evidence for a submissive pheromone

One hundred and two prepubertal pigs were used in two experiments to determine if adrenocorticotropin hormone (ACTH)-induced increase in submissive behavior could be mediated by odorous signals. In experiment one, urine was collected from pigs treated with either 0, 1 or 10 IU/kg ACTH. Urine from pigs given 1.0 IU/kg ACTH caused a trend for a rise in submissive behavior. Level of plasma cortisol from donor pigs correlated well (r = .92) with duration of submissive behavior in the tested pigs. In experiment two, urine from ACTH-treated pigs increased submissive behavior when sprayed in the air during late fight. Thus, ACTH-induced submissiveness may be mediated by a pheromone. These results fit the hypothesis that, in addition to visual cues, an olfactory cue (perhaps adrenal in origin) is released towards the end of a fight to signal submission. Aerosolizing urine from ACTH-treated pigs may have interfered with this pheromonal signal.     

The use of tactile and olfactory cues in neonatal orientation and localization of the nipple

A good deal of effort has been directed toward determining the sensory cues employed by neonatal animals in orienting to, and localizing, the nipple. The results of previous studies are contradictory. Some investigators have claimed that olfactory cues are critical, while others suggest that tactile cues are of primary importance in these behaviors. The present studies indicate that, in kittens, there are two essential components of the suckling process: orientation to the mother and localization of the nipple. In these experiments, the ability and time involved in localizing and attaching to the nipple of the anesthetized mother were measured in several conditions. With tactile input impaired, kittens had no difficulty locating the mother, but could not locate the nipple. In contrast, olfactory disruption nerver impaired nipple localization and attachment when the kitten was in contact with the mother, but interfered with the kitten's ability to locate the mother when removed from her. These data suggest that olfactory cues are employed in locating the mother, and tactile cues from the perioral region are employed in locating the nipple.     

Hedonic reactivity to visual and olfactory cues: rapid facial electromyographic reactions are altered in anorexia nervosa

Though it has been suggested that hedonic processing is altered in anorexia nervosa (AN), few studies have used objective measures to assess affective processes in this eating disorder. Accordingly, we investigated facial electromyographic, autonomic and subjective reactivity to the smell and sight of food and non-food stimuli, and assessed more particularly rapid facial reactions reflecting automatic processing of pleasantness. AN and healthy control (HC) women were exposed, before and after a standardized lunch, to pictures and odorants of foods differing in energy density, as well as to non-food sensory cues. Whereas the temporal profile of zygomatic activity in AN patients was typified by a fast drop to sensory cues within the 1000 ms following stimulus onset, HC showed a larger EMG reactivity to pictures in a 800-1000 ms time window. In contrast, pleasantness ratings discriminated the two groups only for high energy density food cues suggesting a partial dissociation between objective and subjective measures of hedonic processes in AN patients. The findings suggest that the automatic processing of pleasantness might be altered in AN, with the sensitivity to reward being modulated by controlled processes.     

Location and features of instructive spatial cues do not influence the time course of covert shifts of visual spatial attention

The time course of shifting visual spatial attention to flickering stimuli in the left and right visual hemifield was investigated. The goal was to test whether an instructive peripheral salient cue located close to the newly to-be-attended location triggers faster shifts per se compared to a central cue. Besides behavioural data an objective electrophysiological measure, the steady-state visual evoked potential (SSVEP) was used to measure the time course of visual pathway facilitation in the human brain for centrally and peripherally cued shifts of spatial attention. Results revealed that both spatial cues resulted in identical time courses of shifts of covert spatial attention. This was true with respect to behavioural data and SSVEP amplitude. Results support the notion that a salient peripheral spatial cue does not automatically produce faster shifts of spatial attention to the to-be-attended location when this cue is informative and embedded in an ongoing stimulation.     

Entorhinal cortex lesions disrupt the transition between the use of intra- and extramaze cues for navigation in the water maze

This study with rats examined the effects of excitotoxic lesions to the entorhinal cortex (EC) and hippocampus (HPC) on using extramaze and intramaze cues to navigate to a hidden platform in a water maze. HPC lesions resulted in a disruption to the use of extramaze cues, but not intramaze cues, whereas EC lesions had no effect on the use of these cues when they were encountered for the first time. However, prior navigation training in which 1 type of cue was relevant disrupted navigation with the other type in rats with EC lesions. Results show that the EC contributes to the processing of spatial information, but that this contribution is most apparent when there is a conflict between 2 sources of navigational cues in the water maze.     

The development of spatial capacity in piloting and dead reckoning by infant rats: use of the huddle as a home base for spatial navigation

Two forms of spatial navigation, piloting using external cues and dead reckoning using self-movement cues, are manifest in the outward and homeward trips of adult rats exploring from a home base. Here, the development of these two forms of spatial behavior are described for rats aged 14-65 days using a new paradigm in which a huddle of pups or an artificial huddle, a small heat pad, served as a home base on an open circular table that the rats could explore. When moving away from both home bases, the travel distance, path complexity, and number of stops of outward trips from the home base increased progressively with age from postnatal day 16 through 22. When returning to the home bases, the return trips to the home base were always more direct and had high travel velocities even though travel distance increased with age for the longest trips. The results are discussed in relation to the ideas that: (1) the pups pilot on the outward portion of their excursion and dead reckon on the homeward portion of their excursion, and (2) the two forms of navigation and associated spatial capacity are interdependent and develop in parallel and in close association with locomotor skill.     

Control of adaptive locomotion: effect of visual obstruction and visual cues in the environment

Visual information regarding obstacle position and size is used for planning and controlling adaptive gait. However, the manner in which visual cues in the environment are used in the control of gait is not fully known. This research examined the effect of obstacle position cues on the lead and trail limb trajectories during obstacle avoidance with and without visual information of the lower limbs and obstacle (termed visual exproprioception). Eight subjects stepped over obstacles under four visual conditions: full vision without obstacle position cues, full vision with position cues, goggles without position cues and goggles with position cues. Goggles obstructed visual exproprioception of the lower limbs and the obstacle. Position cues (2 m tall) were placed beside the obstacle to provide visual cues regarding obstacle position. Obstacle heights were 2, 10, 20 and 30 cm. When wearing goggles and without position cues, a majority of the dependent measures (horizontal distance, toe clearance and lead stride length) increased for the 10, 20 and 30 cm obstacles. Therefore lower limb–obstacle visual exproprioception was important for the control of both limbs, even though with normal vision the trail limb was not visible during obstacle clearance. When wearing goggles, the presence of position cues, which provided on-line visual exproprioception of the self relative to the obstacle position in the anterior–posterior direction, returned lead and trail foot placements to full vision values. Lead toe clearance was not affected by the position cues, trail clearance decreased but was greater than values observed during full vision. Therefore, visual exproprioception of obstacle location, provided by visual cues in the environment, was more relevant than visual exproprioception of the lower limbs for controlling lead and trail foot placement.     

Old age impairs the use of arbitrary visual cues for predictive control of fingertip forces during grasp

Old age impairs the ability to form new associations for declarative memory, but the ability to acquire and retain procedural memories remains relatively intact. Thus, it is unclear whether old age affects the ability to learn the visuomotor associations needed to set efficient fingertip forces for handling familiar objects. We studied the ability for human subjects to use visual cues (color) about the mechanical properties (texture or weight) of a grasped object to control fingertip forces during prehension. Old and young adults (mean age 77 years and 22 years, respectively) grasped and lifted an object that varied in texture at the gripped surfaces (experiment 1: sandpaper versus acetate surface materials) or weight (experiment 2: 200 g versus 400 g). The object was color-coded according to the mechanical property in the "visual cue" condition, and the mechanical property varied unpredictably across lifts in the "no visual cue" condition. In experiment 1 (texture), the young adults' grip force (force normal to the gripped surface) when the object lifted from the support surface was 24% smaller when the surfaces were color-coded. The old adults' grip force did not vary between the visual conditions despite their accurate reports of the grip surface colors prior to each lift. Comparable findings were obtained in experiment 2, when object weight was varied and peak grip force rate prior to object lift-off was measured. Furthermore old and young subjects alike used about 2 N of grip force when lifting the 200 g object in experiment 2. Therefore, the old adults' failure to adjust grip force when the color cue was present cannot be attributed to a general inability or unwillingness to use low grip force when handling objects. We conclude that old age affects the associative learning that links visual identification of an object with the fingertip forces for efficiently handling the object. In contrast, old and young subjects' grip force was influenced by the preceding lift, regardless of visual cues, which supports existing theories that multiple internal representations govern predictive control of fingertip forces during prehension.     

On-line feedback control of human visually guided slow ramp tracking: effects of spatial separation of visual cues

Galanin-like peptide (GALP) is a newly discovered 60 amino acid peptide from the porcine hypothalamus. GALP has been shown to be expressed predominantly in the arcuate nucleus (ARC) of the rat hypothalamus, a region considered to be one of the most important feeding-regulating centers in the brain. GALP-containing neurons in the ARC express leptin receptors, but relationships between GALP and other feeding-regulating neurons have not yet been fully elucidated. Given that Orexin (OX)-containing neurons make synaptic inputs to the ARC, we thus examined the relationship between GALP and OX in the ARC by use of a dual immunostaining technique. OX-immunoreactive fibers appeared to be closely apposed to GALP-immunoreactive cell bodies and their processes. We also examined whether the OX receptor, OX₁-R was expressed in the GALP-containing neurons. Immunoreactivity for both OX₁-R and GALP was detectable in 9.6 % neurons (range 4.2–14.6%) in the ARC. These findings strongly suggest that GALP may participate in the regulation of feeding behavior under the influence of leptin and OX.     

Integration of haptic and visual size cues in perception and action revealed through cross-modal conflict

We investigated the contribution of haptic and visual information about object size to both perception and action. Kinematics of the right hand were measured while participants performed grasping actions or manual estimations under the guidance of haptic information from the left hand, binocular visual information, or both haptics and vision. The greatest uncertainty was observed with haptic information alone. Moreover, when visual and haptic sizes were congruent, performance was no different from that with vision alone. Although this gives the appearance that vision dominates, when information from the two senses was incongruent, an influence of haptic cues emerged for both tasks. Our paradigm also allowed us to demonstrate that haptic sensitivity, like visual sensitivity, scales with object size for manual estimation (consistent with Weber’s law) but not for grasping. In sum, although haptics represents a less certain source of information, haptic processing follows similar principles to vision and its contribution to perception and action becomes evident only when cross-modal information is incongruent.     

Olfactory cues for oviposition behavior in Toxorhynchites moctezuma and Toxorhynchites amboinensis (Diptera: Culicidae)

In laboratory tests gravid female Toxorhynchites moctezuma (Dyar & Knab) and Toxorhynchites amboinensis (Doleschall) were offered the choice of black oviposition jars containing a diethyl ether extract of water collected from a natural oviposition site for these species (i.e., used tires), a dilution series of 4-methylcyclohexanol, 3-methylindole, 2-methylphenol, 3-methylphenol and 4-methylphenol, or solvent. Tire water extract and all test compounds acted as oviposition attractants and stimulants for both species, with the threshold amounts required to elicit these behaviors varying between the species and among the compounds tested.     

Alcohol aversion generalization in rats: specific disruption of taste and odor cues with gustatory neocortex or olfactory bulb ablations

Rats with ablations of the gustatory neocortex (Experiment 1) and rats with olfactory bulb ablations (Experiment 2) were compared with normal rats for aversion generalization to both single taste solutions (sucrose, sodium chloride, quinine hydrochloride, hydrochloric acid) and compound taste solutions (pairs of the four single tastants) following alcohol aversion training. All rats acquired equal and strong alcohol aversions. Control rats showed consistent aversion generalization to both the sucrose + quinine and the sucrose + hydrochloric acid solutions; no significant generalization occurred to the single tastants except a weak generalization to sucrose in Experiment 2. Rats with gustatory neocortical ablations failed to show aversion generalization to any of the taste solutions. Rats with olfactory bulbectomies displayed the same aversion generalization functions as control rats but exhibited significantly faster extinction of the alcohol aversion than did the trained control rats. Results from the present experiments suggest that during alcohol aversion learning, rats lacking gustatory neocortex use odor cues (no taste generalization), whereas rats lacking olfactory bulbs utilize taste cues (normal taste generalization).     

Learning of olfactory cues is not necessary for early lamb recognition by the mother

Ewes identify their young through the use of different sensory modalities. Olfactory recognition, which mediates selective acceptance at the udder, is established at 4 h postpartum (pp). Visual and auditory cues are involved in recognition at a distance, which is evident at 12 h pp. This study investigates whether anosmic ewes are able (a) to develop visual and auditory recognition and (b) to restore selective acceptance of their lamb at the udder. Visual and auditory recognition was assessed in anosmic and intact ewes at 12 h and 24 h pp by a test of two choices: their own and an alien lamb. Selectivity at allowing suckling was tested by presenting successively an alien and the familiar lamb at 4 h, 3 days, and 1 month pp. In the two-choice recognition test, at both 12 h and 24 h pp, anosmic as well as intact ewes showed a preference for their familiar lamb. Although anosmic ewes showed no difference in their acceptance of alien and familiar lambs for suckling at 4 h and 3 days pp, they nursed the alien lamb less at 1 month pp and showed more rejection behaviors toward it. Thus, visual, auditory, or both those types of recognition can be rapidly established, independent of olfactory recognition. Moreover, differential behavior of anosmic ewes toward their own versus an alien lamb at the udder at 1 month suggests that vision and audition may compensate to some extent for the loss of olfaction.     

Olfactory epithelium and ontogeny of the nasal chambers in the bowhead whale (Balaena mysticetus)

In a species of baleen whale, we identify olfactory epithelium that suggests a functional sense of smell and document the ontogeny of the surrounding olfactory anatomy. Whales must surface to breathe, thereby providing an opportunity to detect airborne odorants. Although many toothed whales (odontocetes) lack olfactory anatomy, baleen whales (mysticetes) have retained theirs. Here, we investigate fetal and postnatal specimens of bowhead whales (Balaena mysticetus). Computed tomography (CT) reveals the presence of nasal passages and nasal chambers with simple ethmoturbinates through ontogeny. Additionally, we describe the dorsal nasal meatuses and olfactory bulb chambers. The cribriform plate has foramina that communicate with the nasal chambers. We show this anatomy within the context of the whole prenatal and postnatal skull. We document the tunnel for the ethmoidal nerve (ethmoid foramen) and the rostrolateral recess of the nasal chamber, which appears postnatally. Bilateral symmetry was apparent in the postnatal nasal chambers. No such symmetry was found prenatally, possibly due to tissue deformation. No nasal air sacs were found in fetal development. Olfactory epithelium, identified histologically, covers at least part of the ethmoturbinates. We identify olfactory epithelium using six explicit criteria of mammalian olfactory epithelium. Immunohistochemistry revealed the presence of olfactory marker protein (OMP), which is only found in mature olfactory sensory neurons. Although it seems that these neurons are scarce in bowhead whales compared to typical terrestrial mammals, our results suggest that bowhead whales have a functional sense of smell, which they may use to find prey.     

Tuning host specificity during the ontogeny of a fish ectoparasite: behavioural responses to host-induced cues

The choice between two alternative hosts, brown trout (Salmo trutta) and roach (Rutilus rutilus), and the response to visual and olfactory cues were studied in the ontogeny of Argulus coregoni. The initial preference of the smallest parasites for brighter roach changed at the age of 2 weeks, at the size of about 2 mm, for trout, a typical salmonid host. Younger argulids were attracted by a non-specific visual stimulus (white disc over dark background), and they did not respond to olfactory stimulation (fish-conditioned water). Later, the response to visual stimuli was modulated by trout-conditioned water, but not by that conditioned by roach. The primary role of vision, particularly in early ontogeny, is emphasized as an adaptation of A. coregoni to habitats in boreal latitudes, clear and running water with a sparse fish population. In sub-adult and adult parasites, vision is complimented by olfaction that enables them to choose hosts more precisely. The nature and adaptive significance of the ontogenetic shift in host choice by A. coregoni is discussed.