Research

Neural Structural Connectivity in Olfactory Spatial Attention

Harshita Chatterjee, Imran shareef Syed, Ganesh Elumalai, Nneoma Osakwe, hari krishna golla, Nadira Sewram, Pradeep Chandrasekhar, Nitya Akarsha Surya Venkat Ghanta, Valencia Brown, Lekesha Sobers


Abstract

Different aspects of spatial neglect, the disability to locate the position of the source of an external stimulus, have been studied frequently especially in regard to lack of response to visual stimuli. Many papers fail to elaborate on the lack of response to auditory stimuli and even less research has been conducted on the extraction of spatial information from olfactory stimuli [1-6]. In this study, we attempted to find a structural connection between the Olfactory Cortex (OC) and Temporoparietal Junction (TPJ) in order to suggest that processed olfactory information is carried from the OC to the TPJ, where the spatial information of the odor may be acquired. Positive results were obtained in all subjects with a lateralization observed in the right hemisphere.

 

Introduction

Olfactory identification involves the coalesced code molded by particular patterns of excitatory input from olfactory receptor neurons. It was suggested that this combinatorial coding mechanism was contributed by the spatiotemporal patterning of active neurons in olfactory centers [1]. The olfactory neural process underlying spatial recognition encompasses the computation of molecular information in constructing an image and possibly the location of a particular odorant [2, 3]. Spatial information may be configured by place cells when a subject is situated in a specific environment with or without visual cues. Place cells are a type of neurons in the hippocampus that fire when a subject is introduced to an environment; this makes the subject cognitively aware of specific locations in the space they are present in. Non-visual modalities such as olfaction provide a constellation of the environment to generate spatial recognition of odorants [3]. The function of the hippocampus while doing the same thing is well explained, especially with experimentation involving the suppression of visual and auditory cues [4]. The temporoparietal junction (TPJ) contributes to spatial recognition in the processing of visual, auditory, and somatosensory stimuli, including information from the thalamus and the limbic system [5]. Research done on monkeys revealed area 7 to be of high importance when it comes to being able to produce deficits in spatial attention. This area in monkeys has been thought to correspond to the angular gyrus (Brodmann area 39) and the supramarginal gyrus (Brodmann area 40) in humans along with the superior temporal gyrus (Brodmann area 22), which suggests visual perception and attention through fibers from the visual cortex and inferior parietal lobe [5-7]. The right hemisphere of the cerebrum containing the TPJ tends to be more specific for spatial intelligence and recognition, since spatial deficits are noted to be seen in patients with right TPJ lesions [8, 9]. Two concepts are introduced in relation to olfactory attention and consciousness: orienting and detecting. Orienting is the ability to align one’s focus to a particular sensory input (overt) or from internal memory (covert), and the detection of such stimuli has to be at a concentration where the nervous system is able to perceive it [10, 11]. Pathways from the piriform cortex to the orbitofrontal cortex are used to process odor information, but literature fails to mention projections to other brain regions in order to achieve spatial recognition [1-3]. Olfaction, in contrast to other sensory inputs, does not pass through the thalamus to obtain such spatial processing. Although processing of odors in relation to spatial recognition commences at the olfactory bulb, the effect of a right resected temporal lobectomy demonstrates a decline in olfactory attention that is necessary for olfactory consciousness. This relation considers the probability that spatial recognition processing does occurs at the TPJ [12]. Extensive studies done to analyze the response of TPJ to auditory and visual stimuli have been conducted, but not much work has been done in order to analyze the effect of olfactory stimuli on response generated by the TPJ in humans. The aim of this study is to provide a structural connection from the olfactory cortex (OC) to the TPJ.

 

Materials and Methods

The data sets have been originally developed and reposted by Massachusetts General Hospital – US Consortium Human Connectome Project (MGH-USC HCP) [13,14]. The present study involves twenty healthy adult data sets (10 males and 10 females, between 20–59 years old; mean age = 30.4). The demographic details of the participants with gender and age are available in the data sharing repository [15].

Fiber tractography, the method used in this study, is an elegant method that can be used to delineate individual fiber tracts from diffusion MRIs. The main process of study uses the “DSI-Studio” software tools for complete pre-processing, fiber tracking, and analysis. The imaging data processing helps to convert the pre-processed raw data to .src file format, which is suitable for further reconstruction process. The reconstruction of .src files is achieved through the tools of a software. It converts the .src imaging data to .fib file format. Only the .fib files are compatible for fiber tracking. To delineate individual fiber tracts from reconstructed diffusion images (.fib file), DSI studio software tools were used.
 

Result

The results have been divided into two sets. The first set includes comparison of the different attributes of the fiber tracts found in male and female subjects. The subjects displayed a wide-ranging number of tracts (Graph 1). In the first set of fiber tracing, fibers only extending between merged regions have been considered, since no hemispherical comparison is being made and a primary association is being established before making any classifications.

Number of tracts found in male and female subjects - the difference in the average of the two samples (male and female) was assessed through a t-test calculation. The results signified no clinically important difference. In this study, we suggest that the number of fibers may be directly proportional to the amount of attention drawn towards an olfactory stimulus.

Comparison of the mean length of tracts - the p-value is 0.84. The result is not significant. The lengths of the fibers also show no major difference in the sexes. Comparison of volume of tracts found in the merged regions in male and female subjects - the p-value is 0.94. The result is not significant.

The second set includes a hemispherical comparison of the fibers as seen collectively and in both the male and female subjects. This set of results was derived from tracing fibers extending from mOC to lTPJ and rTPJ. Figure 3 displays results acquired from one of the ten subjects.

Comparison of number of tracts was recorded with a p-value of 0.00. The result is significant. Comparison of the volume of tracts was recorded with a p-value of 0.00. The result is significant.

Discussion

The present study performs tractography in order to establish a neural structural connectivity between the OC and TPJ, and it performs comparative analysis between sexes and hemispheres. Our initial hypothesis suggested that there exists a structural connectivity between the regions which facilitates orientation guided by odor-stimulated spatial attention. Our first set of results upholds the same. We noted a vast range of fibers ranging from 2 to 256. We followed up our findings with a comparison between the sexes and found no significant difference between the number, mean length, or volume of fibers running from the mOC to mTPJ. Our secondary hypothesis suggested that there would be a difference in the connectivity when compared between the hemispheres. In the second set of results, we observe that a significant difference exists in the number and volume of tracts ending in the two hemispheres, favorably lateralized to the right hemisphere. This upholds our secondary hypothesis as well.

In studies conducted in the past, it has been established that when spatial cues are applied in order to assess the attention drawn towards them in response, results are remarkably stable and no differences are observed when compared between sexes [16]. In some studies, while assessing the behavioral response time to stimuli (mostly visual), women were seen responding slower than men but the statistical analysis performed to determine the significance in the difference stated that the difference between men and women was not very significant [17-19]. This could be parallel to spatial attention in response to olfactory stimuli as well.

Differences in cerebral hemispheres indicate different roles in relation to event order [20]. Results show few fibers from the rTPJ decussating to the lTPJ. It was mentioned that TPJ is involved in lower-level computational processes and spatial attention orientation, visual search duration, and theory of the mind and empathy [21-23]. Damage to this area affects awareness of one’s self and causes disorders associated with body knowledge, including out-of-body experiences with respect to experienced unity, self-location, and egocentric visuospatial perspective [21, 24, 25]. Left hemispatial neglect was seen in stroke patients with lesions to the right angular gyrus [26]. This spatial overlap is crucial in interactions between word production and word perception [27]. Due to this relation, it is likely that the rTPJ contributes to olfactory spatial attention of lTPJ.

The lTPJ is comprised of Wernicke’s area, which is responsible for language comprehension, semantic knowledge of single words, pre-semantic processing of faces and names, low-level social perception, and high-level social reasoning [22, 27, 28]. Damage to the lTPJ causes Wernicke’s aphasia and disrupts cognitive processes of the mental state, such as someone’s belief [22, 29]. The lTPJ also encodes multisensorial (eg. visual and auditory) temporal order judgement (TOJ), serving as an integral part of the ‘when’ pathway. This allows an individual to process the timings of two spatially discrete stimuli. The conduction of this experiment was used to assess TOJ by allowing patients to perform two tasks that differentiated temporal order and spatial properties. This is useful in the sense of investigating perception for subjective simultaneity (bias) and noticeable difference (sensitivity). It is known  that the temporal order judgment of visual stimuli is impacted by the detection and identification expedited by attention. The planning of production of saccades towards a specific location in response to a particular stimulus, for example of a dual task paradigm, influences increasing speed of perceptual processing. With this given information, one can deduce that the perception processing of a stimulus occurs first and then temporal order judgement second. This relates to the topic at hand, for TOJ is influenced greatly by spatial attention [22, 29, 30]. Results showing fibers decussating from the rTPJ to the lTPJ were hypothesized by the current researchers contributing to the ‘when’ pathway of olfactory stimuli. The rTPJ spatial attentional activity is noted to interfere with temporal order judgement producing biases but does not reduce its performance. For an unbiased result in TOJ assessment, one has to withstand any spatially induced stimuli or attentional variables that may trigger the involvement of rTPJ. Research has indicated that the ‘what,’ ‘where,’ and ‘when’ processing streams are identical and follow the same organization [21].



    Harshita Chatterjee

    Harshita Chatterjee


    This author has not yet uploaded a bio.

    Imran shareef Syed

    Imran shareef Syed


    This author has not yet uploaded a bio.

    Ganesh Elumalai

    Ganesh Elumalai


    This author has not yet uploaded a bio.

    Nneoma Osakwe

    Nneoma Osakwe


    This author has not yet uploaded a bio.

    hari krishna golla

    hari krishna golla


    This author has not yet uploaded a bio.

    Nadira Sewram

    Nadira Sewram


    Junior Researcher - Department of Neuroscience, Texila American University (Guyana Campus)

    Pradeep Chandrasekhar

    Pradeep Chandrasekhar


    This author has not yet uploaded a bio.

    Nitya Akarsha Surya Venkat Ghanta

    Nitya Akarsha Surya Venkat Ghanta


    Nitya Akarsha Surya Venkat Ghanta,M.D.

    Valencia Brown

    Valencia Brown


    Valencia Brown is a medical student and also a young researcher who studies at the Texila American University in Guyana, and has main interest in the area of neuroscience and its related topics.

    Lekesha Sobers

    Lekesha Sobers


    Guyanese/Saint Lucian BSc. Medical Technology Medical Student