John L. Kubie

A driveable bundle of microwires for collecting single-unit data from freely-moving rats☆

A technique is described for making a sturdy, driveable electrode array of ten fine wires. This moveable array is a modification of a stationary electrode [4]. It has a number of notable advantages over other electrodes designed for recording single-unit activity in freely-moving small mammals. With this electrode many single cells can be recorded in each animal, cells can be held for many days, and recording quality is very good.

Chemical access to the vomeronasal organs of garter snakes

Abstract Garter snakes tongue-flicked cotton swabs soaked in a mixture of earthworm extract and 3H-proline. In snakes with intact tongues and patent vomeronasal ducts, large accumulations of radioactive material, as revealed by autoradiography, were observed in the vomeronasal organs. When the vomeronasal ducts were sutured closed, no radioactivity was discerned in the vomeronasal organs. The accumulations of radioactive material in the organs were reduced slightly when the tongue tips were removed. In snakes whose entire tongue was removed, but whose lips touched the swabs, a discernable amount of radioactive accumulation still occurred in the vomeronasal organs.

The role of the ophidian vomeronasal system in species-typical behavior

The garter snake vomeronasal system is critically involved in several species-typical behaviors including response to female sex pheromones, aggregation, shelter selection, prey selection, prey trailing and prey attack. There is also some evidence that vomeronasal stimulation may be inherently reinforcing.

Snake Tongue Flicking Behavior: Clues to Vomeronasal System Functions

For the past ten years we have been studying the function of the garter snake vomeronasal system. The snake vomeronasal organ is remarkably large and contains more sensory neurons than the snake’s main olfactory apparatus. It appears to detect sexual scents, conspecific scents, and prey odors. These odors are critically important in mating, aggregation,prey trailing, prey attack and prey ingestion (Burghardt & Pruitt, 1975; Halpern & Frumin, 1979; Heller & Halpern, 1983; Kubie & Halpern, 1979; Kubie, Vagvolgyi & Halpern, 1978; Wilde, 1938). The snake vomeronasal organ is situated in a rather odd position for an external chemoreceptor: the walnut-shaped organs sit paramidline above the roof of the mouth and the tiny openings are not directed towards the outside world (or the nasal cavity, as in many vertebrates) but downward towards the roof of the mouth.

Heading-Vector Navigation Based on Head-Direction Cells and Path Integration

Insect navigation is guided by heading vectors that are computed by path integration. Mammalian navigation models, on the other hand, are typically based on map‐like place representations provided by hippocampal place cells. Such models compute optimal routes as a continuous series of locations that connect the current location to a goal. We propose a “heading‐vector” model in which head‐direction cells or their derivatives serve both as key elements in constructing the optimal route and as the straight‐line guidance during route execution. The model is based on a memory structure termed the “shortcut matrix,” which is constructed during the initial exploration of an environment when a set of shortcut vectors between sequential pairs of visited waypoint locations is stored. A mechanism is proposed for calculating and storing these vectors that relies on a hypothesized cell type termed an “accumulating head‐direction cell.” Following exploration, shortcut vectors connecting all pairs of waypoint locations are computed by vector arithmetic and stored in the shortcut matrix. On re‐entry, when local view or place representations query the shortcut matrix with a current waypoint and goal, a shortcut trajectory is retrieved. Since the trajectory direction is in head‐direction compass coordinates, navigation is accomplished by tracking the firing of head‐direction cells that are tuned to the heading angle. Section 1 of the manuscript describes the properties of accumulating head‐direction cells. It then shows how accumulating head‐direction cells can store local vectors and perform vector arithmetic to perform path‐integration‐based homing. Section 2 describes the construction and use of the shortcut matrix for computing direct paths between any pair of locations that have been registered in the shortcut matrix. In the discussion, we analyze the advantages of heading‐based navigation over map‐based navigation. Finally, we survey behavioral evidence that nonhippocampal, heading‐based navigation is used in small mammals and humans.

Linear Look-Ahead in Conjunctive Cells: An Entorhinal Mechanism for Vector-Based Navigation

The crisp organization of the “firing bumps” of entorhinal grid cells and conjunctive cells leads to the notion that the entorhinal cortex may compute linear navigation routes. Specifically, we propose a process, termed “linear look-ahead,” by which a stationary animal could compute a series of locations in the direction it is facing. We speculate that this computation could be achieved through learned patterns of connection strengths among entorhinal neurons. This paper has three sections. First, we describe the minimal grid cell properties that will be built into our network. Specifically, the network relies on “rigid modules” of neurons, where all members have identical grid scale and orientation, but differ in spatial phase. Additionally, these neurons must be densely interconnected with synapses that are modifiable early in the animal’s life. Second, we investigate whether plasticity during short bouts of locomotion could induce patterns of connections amongst grid cells or conjunctive cells. Finally, we run a simulation to test whether the learned connection patterns can exhibit linear look-ahead. Our results are straightforward. A simulated 30-min walk produces weak strengthening of synapses between grid cells that do not support linear look-ahead. Similar training in a conjunctive cell module produces a small subset of very strong connections between cells. These strong pairs have three properties: the pre- and post-synaptic cells have similar heading direction. The cell pairs have neighboring grid bumps. Finally, the spatial offset of firing bumps of the cell pair is in the direction of the common heading preference. Such a module can produce strong and accurate linear look-ahead starting in any location and extending in any direction. We speculate that this process may: (1) compute linear paths to goals; (2) update grid cell firing during navigation; and (3) stabilize the rigid modules of grid cells and conjunctive cells.

Shedding enhances the sexual attractiveness of oestradiol treated garter snakes and their untreated penmates

The courtship behaviour of male garter snakes (Thamnophis radix) was tested with females who received or did not receive oestradiol benzoate (EB) injections prior to shedding, and with non-shedding females who received EB. Each female injected for 5 or more days prior to shedding was courted only after the shed. In addition, most penmates of the EB treated shedders were courted frequently after the treated female shed. Females who received no EB prior to shed showed little or no increase in sexual attractiveness. EB treated females who did not shed were inconsistently courted. It is most likely that shedding potentiates the release of a sexual pheromone from the dorsal skin of EB treated females, and this pheromone can then be spread to the backs of penmates.

Electrophysiological analysis of the nasal chemical senses in garter snakes

Electroolfactogram and electrovomeronasogram recordings were made from garter snakes stimulated with vapor of amyl acetate, butanol and of earthworm wash. The olfactory epithelium was more sensitive than the vomeronasal epithelium to all three stimuli. Volatiles from prey washes were capable of stimulating the olfactory epithelium when delivered as airstreams. The vomeronasal epithelium was sensitive only to the air delivery of vapor of amyl acetate. Single unit recordings from the mitral cell layer of the accessory olfactory bulb of garter snakes were made in response to liquid delivery of a variety of chemical stimuli including classical odorants, amino acids and proteins derived from prey. All three classes of stimuli altered unit firing in the accessory olfactory bulb. Amyl acetate, earthworm wash, goldfish wash and non-volatile amino acids delivered as liquid stimuli to the vomeronasal epithelium produced responses in the accessory olfactory bulb that were more distinct and reliable than the electrovomeronasogram responses to airborne odorants recorded at the periphery. Both excitatory and inhibitory responses were observed in the accessory olfactory bulb of garter snakes. The direction of the response to a given stimulus differed for different neurons. Responses were frequently biphasic and could last longer than 50 seconds. Individual neurons responded to different classes of stimuli suggesting that they are broadly tuned.

Recurrent seizures induce a reversible impairment in a spatial hidden goal task

A major question concerning the learning and memory deficits characteristic of epilepsy is the relative importance of the initial insult that leads to recurrent, unprovoked seizures versus the seizures themselves. A related issue is whether seizure‐induced cognitive decline is permanent or reversible when convulsions cease. To address these problems, adult rats were extensively trained in the “spatial accuracy task,” a dry‐land analog of the Morris water maze. This task allows the rats estimate of the location of a hidden goal zone to be repeatedly measured within each behavioral session. One aim was to measure, in well‐trained animals, the time course of any cognitive impairment caused by a daily flurothyl‐induced generalized seizure over 11 days. A second aim was to look for possible recovery during 9 subsequent days with no seizures. We saw a cumulative degradation in spatial performance during the seizure days and reversal of the deficit after seizures were stopped such that performance returned to baseline. Interestingly, the rate of learning to an asymptote, the rate of performance decline during one‐per‐day seizures and the rate of relearning during the recovery period were all similar. Given that the hippocampus plays an important role in spatial memory and that it is the brain structure most vulnerable to abnormal excitation the implication is that the hippocampus remains essential for precise spatial navigation even after prolonged training in locating a fixed goal zone. Clinically, this finding questions the assumption that patients who experience seizures should return to a baseline cognitive level within hours.

Robert U. Muller—In memory

Bob Muller, friend, colleague, and place-cell pioneer, died following a heart attack on Sept 16, 2013. He was 71 years old. Figure 1 shows Bob at the early stages of place cell recording. FIGURE 1 Bob and John Kubie (approx. 1985) in the “large rectangle” recording chamber. [Color figure can be viewed in the online issue, which is available at http://wileyonlinelibrary.com.]