Mechanisms of competitive selection: A canonical neural circuit framework.

Competitive selection, the transformation of multiple competing sensory inputs and internal states into a unitary choice, is a fundamental component of animal behavior. Selection behaviors have been studied under several intersecting umbrellas including decision-making, action selection, perceptual categorization, and attentional selection. Neural correlates of these behaviors and computational models have been investigated extensively. However, specific, identifiable neural circuit mechanisms underlying the implementation of selection remain elusive. Here, we employ a first principles approach to map competitive selection explicitly onto neural circuit elements. We decompose selection into six computational primitives, identify demands that their execution places on neural circuit design, and propose a canonical neural circuit framework. The resulting framework has several links to neural literature, indicating its biological feasibility, and has several common elements with prominent computational models, suggesting its generality. We propose that this framework can help catalyze experimental discovery of the neural circuit underpinnings of competitive selection.

Correction to: Multiple levers for overcoming the recalcitrance of lignocellulosic biomass.

[This corrects the article DOI: 10.1186/s13068-019-1353-7.].

Multiple levers for overcoming the recalcitrance of lignocellulosic biomass.

Background: The recalcitrance of cellulosic biomass is widely recognized as a key barrier to cost-effective biological processing to fuels and chemicals, but the relative impacts of physical, chemical and genetic interventions to improve biomass processing singly and in combination have yet to be evaluated systematically. Solubilization of plant cell walls can be enhanced by non-biological augmentation including physical cotreatment and thermochemical pretreatment, the choice of biocatalyst, the choice of plant feedstock, genetic engineering of plants, and choosing feedstocks that are less recalcitrant natural variants. A two-tiered combinatoric investigation of lignocellulosic biomass deconstruction was undertaken with three biocatalysts (Clostridium thermocellum, Caldicellulosiruptor bescii, Novozymes Cellic® Ctec2 and Htec2), three transgenic switchgrass plant lines (COMT, MYB4, GAUT4) and their respective nontransgenic controls, two Populus natural variants, and augmentation of biological attack using either mechanical cotreatment or cosolvent-enhanced lignocellulosic fractionation (CELF) pretreatment. Results: In the absence of augmentation and under the conditions tested, increased total carbohydrate solubilization (TCS) was observed for 8 of the 9 combinations of switchgrass modifications and biocatalysts tested, and statistically significant for five of the combinations. Our results indicate that recalcitrance is not a trait determined by the feedstock only, but instead is coequally determined by the choice of biocatalyst. TCS with C. thermocellum was significantly higher than with the other two biocatalysts. Both CELF pretreatment and cotreatment via continuous ball milling enabled TCS in excess of 90%. Conclusion: Based on our results as well as literature studies, it appears that some form of non-biological augmentation will likely be necessary for the foreseeable future to achieve high TCS for most cellulosic feedstocks. However, our results show that this need not necessarily involve thermochemical processing, and need not necessarily occur prior to biological conversion. Under the conditions tested, the relative magnitude of TCS increase was augmentation > biocatalyst choice > plant choice > plant modification > plant natural variants. In the presence of augmentation, plant modification, plant natural variation, and plant choice exhibited a small, statistically non-significant impact on TCS.

Biomass augmentation through thermochemical pretreatments greatly enhances digestion of switchgrass by Clostridium thermocellum.

BACKGROUND: The thermophilic anaerobic bacterium Clostridium thermocellum is a multifunctional ethanol producer, capable of both saccharification and fermentation, that is central to the consolidated bioprocessing (CBP) approach of converting lignocellulosic biomass to ethanol without external enzyme supplementation. Although CBP organisms have evolved efficient machinery for biomass deconstruction, achieving complete solubilization requires targeted approaches, such as pretreatment, to prepare recalcitrant biomass feedstocks for further biological digestion. Here, differences between how C. thermocellum and fungal cellulases respond to senescent switchgrass prepared by four different pretreatment techniques revealed relationships between biomass substrate composition and its digestion by the two biological approaches. RESULTS: Alamo switchgrass was pretreated using hydrothermal, dilute acid, dilute alkali, and co-solvent-enhanced lignocellulosic fractionation (CELF) pretreatments to produce solids with varying glucan, xylan, and lignin compositions. C. thermocellum achieved highest sugar release and metabolite production from de-lignified switchgrass prepared by CELF and dilute alkali pretreatments demonstrating greater resilience to the presence of hemicellulose sugars than fungal enzymes. 100% glucan solubilization and glucan plus xylan release from switchgrass were achieved using the CELF-CBP combination. Lower glucan solubilization and metabolite production by C. thermocellum was observed on solids prepared by dilute acid and hydrothermal pretreatments with higher xylan removal from switchgrass than lignin removal. Further, C. thermocellum (2% by volume inoculum) showed ~ 48% glucan solubilization compared to < 10% through fungal enzymatic hydrolysis (15 and 65 mg protein/g glucan loadings) of unpretreated switchgrass indicating the effectiveness of C. thermocellum's cellulosome. Overall, C. thermocellum performed equivalent to 65 and better than 15 mg protein/g glucan fungal enzymatic hydrolysis on all substrates except CELF-pretreated substrates. CELF pretreatments of switchgrass produced solids that were highly digestible regardless of whether C. thermocellum or fungal enzymes were chosen. CONCLUSIONS: The unparalleled comprehensive nature of this work with a comparison of four pretreatment and two biological digestion techniques provides a strong platform for future integration of pretreatment with CBP. Lignin removal had a more positive impact on biological digestion of switchgrass than xylan removal from the biomass. However, the impact of switchgrass structural properties, including cellulose, hemicellulose, and lignin characterization, would provide a better understanding of lignocellulose deconstruction.

Adaptive sonar call timing supports target tracking in echolocating bats.

Echolocating bats dynamically adapt the features of their sonar calls as they approach obstacles and track targets. As insectivorous bats forage, they increase sonar call rate with decreasing prey distance, and often embedded in bat insect approach sequences are clusters of sonar sounds, termed sonar sound groups (SSGs). The bat's production of SSGs has been observed in both field and laboratory conditions, and is hypothesized to sharpen spatiotemporal sonar resolution. When insectivorous bats hunt, they may encounter erratically moving prey, which increases the demands on the bat's sonar imaging system. Here, we studied the bat's adaptive vocal behavior in an experimentally controlled insect-tracking task, allowing us to manipulate the predictability of target trajectories and measure the prevalence of SSGs. With this system, we trained bats to remain stationary on a platform and track a moving prey item, whose trajectory was programmed either to approach the bat, or to move back and forth, before arriving at the bat. We manipulated target motion predictability by varying the order in which different target trajectories were presented to the bats. During all trials, we recorded the bat's sonar calls and later analysed the incidence of SSG production during the different target tracking conditions. Our results demonstrate that bats increase the production of SSGs when target unpredictability increases, and decrease the production of SSGs when target motion predictability increases. Furthermore, bats produce the same number of sonar vocalizations irrespective of the target motion predictability, indicating that the animal's temporal clustering of sonar call sequences to produce SSGs is purposeful, and therefore involves sensorimotor planning.

Dynamic representation of 3D auditory space in the midbrain of the free-flying echolocating bat.

Essential to spatial orientation in the natural environment is a dynamic representation of direction and distance to objects. Despite the importance of 3D spatial localization to parse objects in the environment and to guide movement, most neurophysiological investigations of sensory mapping have been limited to studies of restrained subjects, tested with 2D, artificial stimuli. Here, we show for the first time that sensory neurons in the midbrain superior colliculus (SC) of the free-flying echolocating bat encode 3D egocentric space, and that the bat's inspection of objects in the physical environment sharpens tuning of single neurons, and shifts peak responses to represent closer distances. These findings emerged from wireless neural recordings in free-flying bats, in combination with an echo model that computes the animal's instantaneous stimulus space. Our research reveals dynamic 3D space coding in a freely moving mammal engaged in a real-world navigation task.

Sugar yield and composition of tubers from Jerusalem Artichoke (Helianthus tuberosus) irrigated with saline waters.

Currently, major biofuel crops are also food crops that demand fertile soils and good-quality water. Jerusalem artichoke (Helianthus tuberosus, Asteraceae) produces high tonnage of tubers that are rich in sugars, mainly in the form of inulin. In this study, plants of the cultivar "White Fuseau" grown under five salinity levels were evaluated for tuber yield. Results indicated that this cultivar is moderately salt-tolerant if the goal is tuber production. Hydraulic pressings of the tubers produced juice that contained 15% (wet weight) or 55% (dry weight) free sugars, with 70% of these in the form of inulin and the rest as fructose, sucrose, and glucose. Importantly, salinity did not affect the total free sugar or inulin content of the tubers. Tubers were composed of about 12% dry washed bagasse (wet weight) or 44% (dry matter basis) and bagasse retained such high quantities of free sugars after pressing that washing was required for complete sugar recovery. Chemical composition analysis of tuber bagasse suggested that it had low lignin content (11-13 wt%), and its structural sugar composition was similar to chicory root bagasse. Because of the high hemicellulose and pectin content of the bagasse, adding xylanase and pectinase to cellulase substantially improved sugar yields from enzymatic hydrolysis compared to at the same protein loading as cellulase alone. In addition to the high total sugar yield of tuber, these first findings on the sugar and lignin content and enzymatic hydrolysis of tuber bagasse can lead to low-cost production of ethanol for transportation fuels.

Functional Organization and Dynamic Activity in the Superior Colliculus of the Echolocating Bat, Eptesicus fuscus.

Sensory-guided behaviors require the transformation of sensory information into task-specific motor commands. Prior research on sensorimotor integration has emphasized visuomotor processes in the context of simplified orienting movements in controlled laboratory tasks rather than an animal's more complete, natural behavioral repertoire. Here, we conducted a series of neural recording experiments in the midbrain superior colliculus (SC) of echolocating bats engaged in a sonar target-tracking task that invoked dynamic active sensing behaviors. We hypothesized that SC activity in freely behaving animals would reveal dynamic shifts in neural firing patterns within and across sensory, sensorimotor, and premotor layers. We recorded neural activity in the SC of freely echolocating bats (three females and one male) and replicated the general trends reported in other species with sensory responses in the dorsal divisions and premotor activity in ventral divisions of the SC. However, within this coarse functional organization, we discovered that sensory and motor neurons are comingled within layers throughout the volume of the bat SC. In addition, as the bat increased pulse rate adaptively to increase resolution of the target location with closing distance, the activity of sensory and vocal premotor neurons changed such that auditory response times decreased, and vocal premotor lead times shortened. This finding demonstrates that SC activity can be modified dynamically in concert with adaptive behaviors and suggests that an integrated functional organization within SC laminae supports rapid and local integration of sensory and motor signals for natural, adaptive behaviors.SIGNIFICANCE STATEMENT Natural sensory-guided behaviors involve the rapid integration of information from the environment to direct flexible motor actions. The vast majority of research on sensorimotor integration has used artificial stimuli and simplified behaviors, leaving open questions about nervous system function in the context of natural tasks. Our work investigated mechanisms of dynamic sensorimotor feedback control by analyzing patterns of neural activity in the midbrain superior colliculus (SC) of an echolocating bat tracking and intercepting moving prey. Recordings revealed that sensory and motor neurons comingle within laminae of the SC to support rapid sensorimotor integration. Further, we discovered that neural activity in the bat SC changes with dynamic adaptations in the animal's echolocation behavior.

Comparative evaluation of Populus variants total sugar release and structural features following pretreatment and digestion by two distinct biological systems.

BACKGROUND: Populus natural variants have been shown to realize a broad range of sugar yields during saccharification, however, the structural features responsible for higher sugar release from natural variants are not clear. In addition, the sugar release patterns resulting from digestion with two distinct biological systems, fungal enzymes and Clostridium thermocellum, have yet to be evaluated and compared. This study evaluates the effect of structural features of three natural variant Populus lines, which includes the line BESC standard, with respect to the overall process of sugar release for two different biological systems. RESULTS: Populus natural variants, SKWE 24-2 and BESC 876, showed higher sugar release from hydrothermal pretreatment combined with either enzymatic hydrolysis or Clostridium thermocellum fermentation compared to the Populus natural variant, BESC standard. However, C. thermocellum outperformed the fungal cellulases yielding 96.0, 95.5, and 85.9% glucan plus xylan release from SKWE 24-2, BESC 876, and BESC standard, respectively. Among the feedstock properties evaluated, cellulose accessibility and glycome profiling provided insights into factors that govern differences in sugar release between the low recalcitrant lines and the BESC standard line. However, because this distinction was more apparent in the solids after pretreatment than in the untreated biomass, pretreatment was necessary to differentiate recalcitrance among Populus lines. Glycome profiling analysis showed that SKWE 24-2 contained the most loosely bound cell wall glycans, followed by BESC 876, and BESC standard. Additionally, lower molecular weight lignin may be favorable for effective hydrolysis, since C. thermocellum reduced lignin molecular weight more than fungal enzymes across all Populus lines. CONCLUSIONS: Low recalcitrant Populus natural variants, SKWE 24-2 and BESC 876, showed higher sugar yields than BESC standard when hydrothermal pretreatment was combined with biological digestion. However, C. thermocellum was determined to be a more robust and effective biological catalyst than a commercial fungal cellulase cocktail. As anticipated, recalcitrance was not readily predicted through analytical methods that determined structural properties alone. However, combining structural analysis with pretreatment enabled the identification of attributes that govern recalcitrance, namely cellulose accessibility, xylan content in the pretreated solids, and non-cellulosic glycan extractability.

Sensorimotor integration on a rapid time scale.

Sensing is fundamental to the control of movement: From grasping objects to speech production, sensing guides action. So far, most of our knowledge about sensorimotor integration comes from visually guided reaching and oculomotor integration, in which the time course and trajectories of movements can be measured at a high temporal resolution. By contrast, production of vocalizations by humans and animals involves complex and variable actions, and each syllable often lasts a few hundreds of milliseconds, making it difficult to infer underlying neural processes. Here, we measured and modeled the transfer of sensory information into motor commands for vocal amplitude control in response to background noise, also known as the Lombard effect. We exploited the brief vocalizations of echolocating bats to trace the time course of the Lombard effect on a millisecond time scale. Empirical studies revealed that the Lombard effect features a response latency of a mere 30 ms and provided the foundation for the quantitative audiomotor model of the Lombard effect. We show that the Lombard effect operates by continuously integrating the sound pressure level of background noise through temporal summation to guide the extremely rapid vocal-motor adjustments. These findings can now be extended to models and measures of audiomotor integration in other animals, including humans.

Action Enhances Acoustic Cues for 3-D Target Localization by Echolocating Bats.

Under natural conditions, animals encounter a barrage of sensory information from which they must select and interpret biologically relevant signals. Active sensing can facilitate this process by engaging motor systems in the sampling of sensory information. The echolocating bat serves as an excellent model to investigate the coupling between action and sensing because it adaptively controls both the acoustic signals used to probe the environment and movements to receive echoes at the auditory periphery. We report here that the echolocating bat controls the features of its sonar vocalizations in tandem with the positioning of the outer ears to maximize acoustic cues for target detection and localization. The bat's adaptive control of sonar vocalizations and ear positioning occurs on a millisecond timescale to capture spatial information from arriving echoes, as well as on a longer timescale to track target movement. Our results demonstrate that purposeful control over sonar sound production and reception can serve to improve acoustic cues for localization tasks. This finding also highlights the general importance of movement to sensory processing across animal species. Finally, our discoveries point to important parallels between spatial perception by echolocation and vision.

Timing matters: sonar call groups facilitate target localization in bats.

To successfully negotiate a cluttered environment, an echolocating bat must control the timing of motor behaviors in response to dynamic sensory information. Here we detail the big brown bat's adaptive temporal control over sonar call production for tracking prey, moving predictably or unpredictably, under different experimental conditions. We studied the adaptive control of vocal-motor behaviors in free-flying big brown bats, Eptesicus fuscus, as they captured tethered and free-flying insects, in open and cluttered environments. We also studied adaptive sonar behavior in bats trained to track moving targets from a resting position. In each of these experiments, bats adjusted the features of their calls to separate target and clutter. Under many task conditions, flying bats produced prominent sonar sound groups identified as clusters of echolocation pulses with relatively stable intervals, surrounded by longer pulse intervals. In experiments where bats tracked approaching targets from a resting position, bats also produced sonar sound groups, and the prevalence of these sonar sound groups increased when motion of the target was unpredictable. We hypothesize that sonar sound groups produced during flight, and the sonar call doublets produced by a bat tracking a target from a resting position, help the animal resolve dynamic target location and represent the echo scene in greater detail. Collectively, our data reveal adaptive temporal control over sonar call production that allows the bat to negotiate a complex and dynamic environment.