Independent Neural Pathways Research Articles

Sensory discrimination between aversive salty and bitter tastes in an haematophagous insect.

Sensory aversion is essential for avoiding prospective dangers. We studied the chemical perception of aversive compounds of different gustatory modalities (salty, bitter) in the haematophagous bug, Rhodnius prolixus. Over a walking arena, insects avoided a substrate embedded with 1M NaCl or KCl if provided with water as an alternative. However, no preferences were expressed when both salts were opposed to each other. A pre-exposure to amiloride interfered with the repellency of NaCl and KCl equally, suggesting that amiloride-sensitive receptors are involved in the detection of both salts. Discriminative experiments were then performed to determine whether R.prolixus can distinguish between these salts. An aversive operant conditioning involving either NaCl or KCl modulated the repellency of the conditioned salt, but also of the novel salt. Repellency levels of both salts were rigid to a chemical pre-exposure to any of both salts. When gustatory modalities were crossed by presenting as a choice NaCl and a bitter molecule as caffeine (Caf), no innate preferences were expressed. Aversive operant conditionings with either NaCl or Caf rendered unspecific changes in the repellency of both compounds. A chemical pre-exposure to Caf modulated the response to Caf but not to NaCl, suggesting the existence of two independent neural pathways for the detection of salts and bitter compounds. Overall results suggest that R.prolixus cannot discriminate molecules of the same gustatory modality (i.e. salty), but can distinguish between salty and bitter tastes. The potential use of aversive gustatory stimuli as a complement of commercially available olfactory repellents is discussed.

Social Facilitation of Long-Lasting Memory is Mediated by CO <sub>2</sub> in Drosophila

How social interactions influences cognition is a fundamental question, yet rarely addressed at the neurobiological level. It is well established that the presence of conspecifics affects learning and memory performance, but the neural basis for the influence of the social context has received little attention. In the fruitfly Drosophila melanogaster, the presence of conspecifics improves retrieval of a long-lasting olfactory memory. Here, we demonstrate that this memory is composite and involves two independent neural pathways. One is based on the expression of individual memory and depends on the α’β’ lobes outputs of the Mushroom Bodies (MBs), the memory center in the insect brain. The other one relies on the expression of group memory and requires a distinct sub-part of the MBs, the αβ lobes outputs. We show that such social facilitation increases with group size and is triggered by the CO2 released by group members. Among the known neurons carrying CO2 information in the brain, we establish that the bilateral Ventral Projection Neuron (biVPN), which projects onto the MBs, is necessary for social facilitation. Moreover, we demonstrate that this CO2-dependent memory engages a serotoninergic pathway involving the Dorsal-Paired Median neurons (DPM), which reveals a new role for this pair of serotonergic neurons. Overall, we identify both the sensorial cue and the neural circuit (biVPN>αβ>DPM>αβ) governing social facilitation of memory. This study provides the first demonstration that being in a group recruits the expression of a cryptic memory and that variations in CO2 concentration can affect cognitive processes in insects.

Identification of Rubisco anxiolytic-like peptides (rALPs) by comprehensive analysis of spinach green leaf protein digest

Rubisco, an enzyme for photosynthetic carbon dioxide fixation, is a major green leaf protein and known as the most abundant protein on the Earth. We found that Rubisco digested mimicking gastrointestinal enzymatic conditions exhibited anxiolytic-like effects after oral administration in mice. Based on a comprehensive peptide analysis of the digest using nanoLC-Orbitrap-MS and the structure-activity relationship of known anxiolytic-like peptides, we identified SYLPPLTT, SYLPPLT and YHIEPV [termed Rubisco anxiolytic-like peptide (rALP)-1, rALP-1(1–7) and rALP-2, respectively], which exhibited potent anxiolytic-like effects after oral administration. The anxiolytic-like effects of rALP-1/rALP-1(1–7) were blocked by a serotonin 5-HT1A receptor antagonist, whereas rALP-2-induced effects were inhibited by a δ-opioid receptor antagonist. In conclusion, novel Rubisco-derived anxiolytic-like peptides, rALP-1/rALP-1(1–7) and rALP-2, act via independent neural pathways.

Restoring motor control and sensory feedback in people with upper extremity amputations using arrays of 96 microelectrodes implanted in the median and ulnar nerves

Objective. An important goal of neuroprosthetic research is to establish bidirectional communication between the user and new prosthetic limbs that are capable of controlling >20 different movements. One strategy for achieving this goal is to interface the prosthetic limb directly with efferent and afferent fibres in the peripheral nervous system using an array of intrafascicular microelectrodes. This approach would provide access to a large number of independent neural pathways for controlling high degree-of-freedom prosthetic limbs, as well as evoking multiple-complex sensory percepts. Approach. Utah Slanted Electrode Arrays (USEAs, 96 recording/stimulating electrodes) were implanted for 30 days into the median (Subject 1-M, 31 years post-amputation) or ulnar (Subject 2-U, 1.5 years post-amputation) nerves of two amputees. Neural activity was recorded during intended movements of the subject’s phantom fingers and a linear Kalman filter was used to decode the neural data. Microelectrode stimulation of varying amplitudes and frequencies was delivered via single or multiple electrodes to investigate the number, size and quality of sensory percepts that could be evoked. Device performance over time was assessed by measuring: electrode impedances, signal-to-noise ratios (SNRs), stimulation thresholds, number and stability of evoked percepts. Main results. The subjects were able to proportionally, control individual fingers of a virtual robotic hand, with 13 different movements decoded offline (r = 0.48) and two movements decoded online. Electrical stimulation across one USEA evoked >80 sensory percepts. Varying the stimulation parameters modulated percept quality. Devices remained intrafascicularly implanted for the duration of the study with no significant changes in the SNRs or percept thresholds. Significance. This study demonstrated that an array of 96 microelectrodes can be implanted into the human peripheral nervous system for up to 1 month durations. Such an array could provide intuitive control of a virtual prosthetic hand with broad sensory feedback.

Learning from the other limb's experience: sharing the 'trained' M1 representation of the motor sequence knowledge.

Key points Participants were scanned during the untrained‐hand performance of a motor sequence, intensively trained a day earlier, and also a similarly constructed but novel, untrained sequence.The superior performance levels for the trained, compared to the untrained sequence, were associated with a greater magnitude of activity within the primary motor cortex (M1), bilaterally, for the trained sequence.The differential responses in the ‘trained’ M1, ipsilateral to the untrained hand, were positively correlated with experience‐related differences in the functional connectivity between the ‘trained’ M1 and (1) its homologue and (2) the dorsal premotor cortex (PMd) within the contralateral hemisphere.No significant correlation was evident between experience‐related differences in M1 – M1 and M1 – PMd connectivity measures.These results suggest that the transfer of sequence‐specific information between the two primary motor cortices is predominantly mediated by excitatory mechanisms driven by the ‘trained’ M1 via two independent neural pathways.

Dynamic integration of information about salience and value for saccadic eye movements

Humans shift their gaze to a new location several times per second. It is still unclear what determines where they look next. Fixation behavior is influenced by the low-level salience of the visual stimulus, such as luminance, contrast, and color, but also by high-level task demands and prior knowledge. Under natural conditions, different sources of information might conflict with each other and have to be combined. In our paradigm, we trade off visual salience against expected value. We show that both salience and value information influence the saccadic end point within an object, but with different time courses. The relative weights of salience and value are not constant but vary from eye movement to eye movement, depending critically on the availability of the value information at the time when the saccade is programmed. Short-latency saccades are determined mainly by salience, but value information is taken into account for long-latency saccades. We present a model that describes these data by dynamically weighting and integrating detailed topographic maps of visual salience and value. These results support the notion of independent neural pathways for the processing of visual information and value.

The role of dopamine and serotonin in conditioned food aversion learning in the honeybee

For most animals, eating entails the risk of being poisoned. Learning how to identify foods with toxins is an important mechanism that reduces the risk of poisoning. While conditioned food aversions have been studied in vertebrates for over 50 years, the neural circuits underlying this form of learning have been difficult to elucidate because of their complexity. Insects, such as fruit flies and honeybees, are important models for the study of the neural mechanisms of learning and memory, but conditioned food aversions have not yet been reported from either species. My collaborators and I recently established that the honeybee has the ability to learn to avoid odours associated with toxins in food using two independent neural pathways. In these experiments, we found that honeybees can learn to associate scents with toxins that they can pre-ingestively detect using their proboscis. This form of learning is primarily mediated by the neurotransmitter, dopamine. We also found a second mechanism: bees can learn to avoid odours associated with the malaise caused by ingesting toxins. This form of learning is mediated by serotonin. Our data are the first to show that two different mechanisms account for conditioned food aversions in insects.

Phenylephrine into the median raphe nucleus evokes an anxiolytic-like effect in free-feeding rats but does not alter food intake in free feeding rats

This study investigated the role of MnR α 1-adrenergic receptors in the control of anxiety-like and feeding behaviors and attempted to reveal a possible functional association between both behaviors. The α 1-adrenergic agonist phenylephrine (PHE) (at doses of 0.2, 2, 6, 20 nmol) or saline was injected into the MnR or into the pontine nucleus (Pn) of free-feeding rats. The animals were exposed to the elevated plus maze to analyse spatial–temporal and ethological variables. Subsequently, the ingestive and non-ingestive behaviors were recorded during 30 min and feeding and drinking behaviors were measured. Both in the elevated plus-maze and in the feeding chamber, all PHE doses injected into the MnR decreased the risk assessment frequency, an ethological parameter of anxiolytic-like effect. The spatial–temporal variables remained unchanged after PHE treatment. Feeding behavior was not affected by PHE into the MnR. The anxiety-like or ingestive behaviors were not affected by PHE treatment in the Pn, an area adjacent to the MnR. These data indicate that α 1-adrenergic receptors within MnR participate in the control of anxiety-like behaviors. The absence of effects on feeding behavior after MnR α 1-adrenergic activation could be due to an elevated α 1-adrenergic tonus and its possible strong facilitatory influence on 5-HT neurons within MnR. Furthermore, the present results suggest that anxiety-like and feeding behaviors controled by MnR adrenergic circuits operate by independent neural pathways.

Changes in food intake and anxiety-like behaviors after clonidine injected into the median raphe nucleus

Serotonergic neurons in the median raphe nucleus (MnR) are stimulated by α 1-adrenergic agonists and inhibited by α 2 agonists. This study investigated the participation of MnR α 2-adrenergic receptors in the control of anxiety-like behavior and feeding as an attempt to establish a functional association between these behaviors. The α 2-adrenergic agonist clonidine (CLON) was injected into the MnR (0, 0.2, 2, 6, 20 nmol), into the pontine nucleus (Pn) or into the mesencephalic reticular formation (mRt) (0.2, 20 nmol) of free-feeding rats. The animals were exposed to the elevated plus-maze to evaluate spatial-temporal and ethological variables. Subsequently, the ingestive and non-ingestive behaviors were recorded during 30 min and the quantity of food and water consumed were measured. The lowest dose of CLON injected into the MnR decreased the total risk assessment (TRA) frequency, an ethological parameter of anxiolytic-like effect, but did not change feeding behavior. The highest dose of CLON injected into the MnR increased the TRA frequency, an anxiogenic-like effect. Similar result was observed after CLON injected into the Pn and mRt at the highest dose. In addition, clonidine at the highest dose caused hyperphagy accompanied by a reduction in the latency to start eating and an increase in feeding frequency when injected into the MnR but not in the Pn or mRt. These data indicate that MnR α 2-adrenergic receptors participate in the control of anxiety-like and feeding behaviors, probably decreasing the facilitatory influence on MnR serotonergic neurons. The present results suggest that these behaviors involve independent neural pathways.

Independent vasomotor control of rat tail and proximal hairy skin

Quantitative differences are known to exist between the vasomotor control of hairy and hairless skin, but it is unknown whether they are regulated by common central mechanisms. We made simultaneous recordings from sympathetic cutaneous vasoconstrictor (CVC-type) fibres supplying back skin (hairy) and tail (hairless) in urethane-anaesthetized, artificially ventilated rats. The animal's trunk was shaved and encased in a water-perfused jacket. Both tail and back skin CVC-type fibres were activated by cooling the trunk skin, and independently by the resultant fall in core (rectal) temperature, but their thresholds for activation differed (skin temperatures 38.8 +/- 0.4 degrees C versus 36.8 +/- 0.4 degrees C, core temperatures 38.1 +/- 0.2 degrees C versus 36.8 +/- 0.2 degrees C, respectively; P < 0.01). Back skin CVC-type fibres were more responsive to skin than to core cooling, while the reverse applied to tail fibres. Back skin CVC-type fibres were less responsive than tail fibres to prostaglandin E2 (PGE2) microinjected into the preoptic area. Spectral analysis showed no significant coherence between tail and back skin CVC-type fibre activities during cooling. After preoptic PGE2 injection, a coherent peak at 1 Hz appeared in some animals; this disappeared after partialization with respect to ventilatory pressure, indicating that it was attributable to common ventilatory modulation. Neuronal inhibition in the rostral medullary raphé by microinjected muscimol (2 mM, 60-120 nl) suppressed both tail and back skin CVC-type fibre activities, and prevented their responses to subsequent skin cooling. These results indicate that thermoregulatory responses of hairless and hairy skin vessels are controlled by independent neural pathways, although both depend on synaptic relays in the medullary raphé.

Are different affordances subserved by different neural pathways?

This paper questions whether affordances are allied exclusively to dorsal stream processing within the visual system, or whether in fact different affordances are subserved by functionally independent neural pathways. Using case study evidence from patients with various visual pathologies, I argue that affordances can be categorised into type based upon their respective neurological underpinning. Such categorisation has implications for the extent to which affordances are consciously perceived or non-consciously ‘picked up’ within the optic array, as well as whether they indicate merely potentials for action or provide necessary information in the actualisation of behaviour.

Synergy of features enables detection of texture defined figures

Traditional theories of early visual processing suggest that elementary visual features are handled in parallel by independent neural pathways. We studied the interaction of orientation and spatial frequency in the discrimination of Gabor random fields. Target textures differed from reference textures either in mean feature value, showing an edge-like transition between both textures (edge defined), or in the degree of feature homogeneity with smooth transitions (region defined). Irrespective of the kind of texture definition, we found strong cue summation for targets defined by both cues simultaneously, provided two conditions were fulfilled. First, they were barely discriminable when defined by one cue alone. Second, the target elements formed a closed 2D surface. Only marginal cue summation was observed when target elements were heterogeneously distributed in a predefined area, lacking a clear 2D shape. Our findings indicate that feature synergy enables figure-ground segregation when the information from independent feature-specific pathways is insufficient for solving this task.

An Argument for Using Ethologically “Natural” Behaviors as Estimates of Unobservable Sensory Processes. Focus on “Sound Localization Performance in the Cat: The Effect of Restraining the Head”

A major goal of systems neuroscience is to describe neural representations of the environment that mediate perception. An experimental strategy adopted by researchers involved in this effort is to obtain three-dimensional correlations between the physical properties of a stimulus, a psychophysical report of the subject, and measures of intervening neural events. Perception is, of course, a private event and objective indirect measures of the percept are obtained. Experiments related to the perceived location of a stimulus often ask subjects to point to the stimulus or to orient to it with an eye movement. Studies using orienting eye movements as the behavioral index of perceived location have become more common now that precise and accurate methods of measuring eye position are readily available. In this issue, Tollin et al. (p. 1223–1234) report that orienting movements of the eyes in head-restrained cats significantly underestimate the actual ability of the animals to localize auditory and visual targets. The target paper compares two commonly used methods of measuring the accuracy and precision of the localization of visual and auditory targets in the cat: eye saccades in animals with their heads restrained and combined eye-head movements (gaze saccades) in animals without head restraint. The effects of stimulus duration were also examined. The shortest-duration stimuli were no longer present when the orienting movement began, and therefore the change in gaze position may have been based on a stored representation of the spatial location of the target. With long-duration stimuli, the stimuli were still present after the orienting movements began and dynamic sensory processing could influence movement accuracy. Target location varied in both azimuth and elevation. Because independent neural pathways that depend on different spatial cues are used to compute the azimuth and elevation of acoustic stimuli (see Zwiers et al. 2003 for a summary of relevant data), the effects of head restraint on localization were analyzed separately for azimuth and elevation. Localization accuracy of both visual and auditory targets improved when measured using a combination of eye and head movements. The effects were not small. When brief stimuli were presented 9 and 18° along the azimuth from the central fixation target, head-restrained animals mislocalized visual and auditory targets by an average of 6.73 and 7.24°, respectively. When the head was not restrained, these values dropped to 1.21 and 0.15°. Improvement was greatest for the shortest-duration stimuli, not the longer duration stimuli that allowed dynamic processing during the orienting move

The neural basis of predicate-argument structure.

Neural correlates exist for a basic component of logical formulae, PREDICATE(x). Vision and audition research in primates and humans shows two independent neural pathways; one locates objects in body-centered space, the other attributes properties, such as colour, to objects. In vision these are the dorsal and ventral pathways. In audition, similarly separable "where" and "what" pathways exist. PREDICATE(x) is a schematic representation of the brain's integration of the two processes of delivery by the senses of the location of an arbitrary referent object, mapped in parietal cortex, and analysis of the properties of the referent by perceptual subsystems. The brain computes actions using a few "deictic" variables pointing to objects. Parallels exist between such nonlinguistic variables and linguistic deictic devices. Indexicality and reference have linguistic and nonlinguistic (e.g., visual) versions, sharing the concept of attention. The individual variables of logical formulae are interpreted as corresponding to these mental variables. In computing action, the deictic variables are linked with "semantic" information about the objects, corresponding to logical predicates. Mental scene descriptions are necessary for practical tasks of primates, and preexist language phylogenetically. The type of scene descriptions used by nonhuman primates would be reused for more complex cognitive, ultimately linguistic, purposes. The provision by the brain's sensory/perceptual systems of about four variables for temporary assignment to objects, and the separate processes of perceptual categorization of the objects so identified, constitute a pre-adaptive platform on which an early system for the linguistic description of scenes developed.

Hierarchy of Habituation Induced by Mechanical Stimuli in Caenorhabditis elegans

C. elegans becomes habituated to repetitive mechanical stimuli. We compared the habituated states induced by three types of mechanical stimuli: touch on the head (head-touch), touch on the anterior body (body-touch), and mechanical tapping of the Petri dish, all of which evoke backward movement. The habituation patterns were similar, but differed in retention period and/or the rate of recovery. We found a hierarchy between the habituated states induced by the three types of mechanical stimuli in the decreasing order of head-touch, body-touch, and tap stimulus. Evidence is presented that the hierarchy is brought out by the magnitude of stimuli rather than by independent neural pathways.

An Introduction to the Biology of Vision

Anyone who has attended a meeting of the Association for Research in Vision and Ophthalmology has probably felt overwhelmed by the explosion of knowledge in the visual neurosciences. The pace of things began to accelerate some time in the early 1960s, when Hubel and Weisel began to unravel the neuronal events that encode complex visual stimuli. This was the beginning of our understanding of parallel processing in the visual system—the concept that various characteristics of visual stimuli, including shape, size, orientation, and color, are extracted by independent neural pathways and recombined at a higher level. It was also the beginning of our understanding of plasticity in the developing visual system, and of the effects of visual deprivation. The breadth and depth of knowledge in these new areas is now so great that it is difficult for a newcomer to know where to start. Many clinical texts unfortunately only impart

Substance P- and Vasoactive Intestinal Peptide-Containing Fibers Reach the Ovary by Independent Routes

The immature rat ovary is innervated by both substance P (SP)- and vasoactive intestinal peptide (VIP)-containing nerve fibers. To determine the origin of these fibers, juvenile rats were sham operated or subjected to transection of the abdominal vagus nerves, superior ovarian nerves, or ovarian plexus nerves or to concomitant transection of the vagal and superior ovarian nerves. Specific immunofluorescent staining of ovarian sections for SP and VIP revealed that VIP innervation to the ovary occurs only via the superior ovarian nerves, whereas ovarian SP innervation is exclusively via the plexus nerves. Thus, specific SP and VIP nerves reach the gland via anatomically different routes. The results indicate that autonomic regulation of ovarian function may be exerted via independent peptidergic neural pathways.

Effects of halothane on the vestibulo-ocular reflex

The differential effect of halothane on the characteristics of fast and slow components of vestibular nystagmus was investigated in rabbits. Eye movements were monitored using the "magnetic search coil" method and evaluated with the aid of a laboratory minicomputer. Low concentrations of halothane act preferentially on the fast component. There is a shift of the position threshold of fast component generation toward the periphery of the orbit and a diminution of the eye velocity during this nystagmus phase. Higher steady state concentrations of halothane reduced the velocity of the slow components whereby there is an increase in the amplitude of stimulation necessary to produce vestibulo-ocular responses of a magnitude to exceed the threshold of fast components. The results support the hypothesis that there are independent neural pathways for the production of fast and slow components of nystagmus whose neurons have different sensitivities to anesthetic agents.