Chapter 9 Refinement of Synaptic Connections

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1 Chapter 9 Refinement of Synaptic Connections

2 Afferent Projection Error during Development During development there is a constant rearrangement of synaptic connections, new synapses are formed and old synapses may be eliminated

3 Afferent Projection Error during Development During development there is a constant rearrangement of synaptic connections, new synapses are formed and old synapses may be eliminated. These changes allow rearrangement of receptive fields and higher accuracy of sensory perception

4 Afferent Projection Error during Development Two types of projections error occur during development: 1) Axons may project to the correct target but they may spread out too far (lack precision). For example, temporal retinal axons projecting to the anterior tectum may send projections outside their main area of innervation (overshoot the target) 2) Postsynaptic neuron or traget receive inputs from the wrong number of afferents. For example at the NMJ

5 Afferent Projection Error during Development Polyneuronal innervation during early embryonic development Mature muscle At the NMJ, each muscle fiber receives an input from only one motoneuron but during early development each fiber is innervated by multiple motoneurons

6 Afferent Projection Error during Development As the result of projection errors, synapse elimination take places in many parts of the developing nervous system How can we determine whether a loss of synapses occur during development?

7 Afferent Projection Error during Development Three main techniques can be use to detect synapse elimination: 1) Intracellular recordings 2) Anatomical studies 3) Study the response of single neurons to afferent stimulation

8 Study of Synapse Elimination by Intracellular Recordings Intracellular recordings can be use to detect the number of synaptic connections based on the assumption that each axon will evoke one PSP upon stimulation

9 Study of Synapse Elimination by Intracellular Recordings Intracellular recordings can be use to detect the number of synaptic connections based on the assumption that each axon will evoke one postsynaptic potential (PSP) upon stimulation At the NMJ stimulation of afferent projections induce a grade response in immature animals that is loss in mature subjects

10 Does Synaptic Elimination Occur in Central Synapses? In the CNS, neurons can make hundreds of connections. How can we study synapse elimination under these conditions? Since the amplitude of the PSP is too small intracellular recording can not provide a clear answer One approach is to count the number of synapse using immunohistochemisty

11 Does Synaptic Elimination Occur in Central Synapses? The process of synapse elimination can be demonstrated by double labeling of commissural neurons in the brain If a dye is injected in a particular area of the brain at postnatal day 2 (P2) and then a different dye is injected (at the same site) at P21, we can determine whether synaptic connections were loss by looking for cells labeled at P2 but not at P22

12 Synaptic Elimination in the Developing Visual System Retinal ganglion cells send axons to the LGN. Neurons in the LGN then project to layer IV of the visual cortex forming segregated eye-specific termination zones called ocular dominance columns or stripes Injection of radiolabeled proline in the eye indicates that during early development projections from one eyes are very widespread

13 Synaptic Elimination in the Developing Visual System Over several weeks of development the initial widespread innervation breaks into discreet patches that represent eye-specific termination zones Functionally this can also be confirmed by electrophysiological recordings in the visual cortex following light stimulation of the retina

14 What factors regulate synapse elimination in the visual system? Electrical activity regulates the elimination of inappropriate synapse and the formation of ocular dominance columns In the retina, spontaneous electrical activity appears before synaptic connections are established in the visual cortex. Does inhibition of spontaneous electrical activity prevent formation of ocular dominance columns?

15 What factors regulate synapse elimination in the visual system? Inhibition of spontaneous electrical activity in the retina with the sodium channel blocker TTX prevent formation of ocular dominance columns

16 What factors regulate synapse elimination in the visual system? Spontaneous electrical activity in the retina of ferrets can be recorded in isolated preparations using a microarray of electrodes or intracellular recordings Retinal explants or the entire retinogeniculate pathway can generate spontaneous electrical activity in vitro

17 What factors regulate synapse elimination in the visual system? How does spontaneous electrical activity result in the formation of ocular dominance columns? It appears that the ability of action potentials to arrive at the cortex with certain delay may trigger separation of axonal projections in layer IV

18 Synaptic Elimination in the Developing Visual System Retinal axons also make inappropriate targeting errors in the LGN. Labeling with horse radish peroxidase (HRP) indicates that retinal axons produce a few collaterals in that layer of the LGN that is going to be innervated by the other eye

19 Regulation of Synaptic Connections by Electrical Activity What factors regulate synaptic connections? Use-dependent changes appear to play an important role in remodeling of the nervous system This can be demonstrated by recording from monocular and binocular neurons in the cat visual system

20 Regulation of Synaptic Connections by Electrical Activity In the visual cortex, neurons in layer IV receive projections from one eye or the other. Therefore, they are called monocular neurons Neurons in other layers (like layer V) respond to stimulation of both eyes and are called binocular neurons

21 Regulation of Synaptic Connections by Electrical Activity Extracellular recordings with an electrode that passed tangentially through the cortex indicated that the majority of neurons are binocular in a normal cat

22 Regulation of Synaptic Connections by Electrical Activity However, following closure of one eye (also know as monocular deprivation) can result in a significant change in the ratio of binocular/monocular neurons in the visual cortex. Under monocular deprivation the majority of neurons become monocular

23 Regulation of Synaptic Connections by Electrical Activity This suggest that the total amount of evoked activity does not predict the strength of a synapse So, does disuse weaken the synapses from the deprived eye? Closure of both eyes (binocular deprivation) does not result in any changes in the ration of binocular/monocular neurons. In this case the majority of the neurons are binocular

24 Regulation of Synaptic Connections by Electrical Activity The strength of a synapse is determined by the differences in the amount of synaptic activity. This is also known as the competition hypothesis.

25 Regulation of Synaptic Connections by Electrical Activity The strength of a synapse is determined by the differences in the amount of synaptic activity. This is also known as the competition hypothesis. In monocular deprive animals cortical neurons receive two different sets of stimulation. In control or binocular deprived animals there is no change in the synaptic activity received from each eye

26 Regulation of Synaptic Connections by Electrical Activity To confirm the competition hypothesis, kittens were rise with artificial strabismus (misalignment of the eyes caused by manipulating one of the ocular muscles). Under this condition visual stimulation activates different positions in the retina so cortical neurons are not activated at the same time. This procedure creates a phase shift in cortical activation coming from different eyes

27 Regulation of Synaptic Connections by Electrical Activity Shift activation of cortical neurons results in the majority of neurons to respond to activation of one eye or the other (monocular activation) This suggest that synapses from each eye must be activated at the same time in order to maintain a strong functional contact with the postsynaptic neuron

28 Regulation of Synaptic Connections by Electrical Activity Electrical activity (use) also regulate the elimination of polyneuronal innervation at the NMJ. In the rat, polyneuronal innervation is eliminated between postnatal dates When a TTX cuff is place around the nerve, removal of polyneuronal innervation is delayed

29 Regulation of Synaptic Connections by Electrical Activity Removal of polyneuronal innervation at the NMJ can be accelerated by increased electrical activity Electrical stimulation of the sciatic nerve accelerated the loss of polyneuronal innervation

30 Sensory Stimulation Regulate Synaptic Rearrangements If electrical activity regulates synaptic strength and elimination, then sensory coding is regulated by experience Experiments in the central auditory system using sound and electrical stimulation have demonstrated changes in sensory coding due to electrical activity

31 Sensory Stimulation Regulate Synaptic Rearrangements In the central auditory system, neurons respond to a limited number of frequencies because the auditory nerve fibers from the cochlea project topographically to the CNS

32 Sensory Stimulation Regulate Synaptic Rearrangements Afferent innervation can be characterized by plotting the range of sound frequencies against the sound intensities that evoked a threshold response. This is called a frequency tuning curve If a narrow area of the cochlea project to a central neurons, the frequency tuning curve recorded from that neurons will be very narrow

33 Sensory Stimulation Regulate Synaptic Rearrangements If a central neuron receives projections from a wider area of the cochlea its frequency tuning curve will be wider Does the temporal pattern of neural activity influences the development of frequency tuning?

34 Sensory Stimulation Regulate Synaptic Rearrangements When mice were reared in a sound environment consisting of repetitive clicks (monotonous stimulation), the frequency tuning curve becomes broader This suggest that when afferents are exposed to identical patterns of stimulation they are unable to segregate along the frequency axis

35 Sensory Stimulation Regulate Synaptic Rearrangements Similar rearrangement of afferent innervation can be obtained in cats that have their cochlea removed and where hair cells are artificially stimulated by electrical pulses It appears that maturation of sensory coding depend on the richness of sensory stimulation

36 Environmental Stimulation Regulate Synaptic Connections Do environmental clues regulate synaptic connections? In many part of the brain neurons respond to stimuli of a specific orientation or to a moving stimuli in a particular direction When kittens are reared in a visual environment of horizontal or vertical stripes, recording from brain neurons indicate that the majority of neurons respond to the stimuli present during rearing

37 Electrical Activity and Alignment of Sensory Maps Often axons project to a particular area forming topographic maps. Electrical activity can regulate the alignment of topographic maps generated on the same target by two different sources of axonal projections

38 Electrical Activity and Alignment of Sensory Maps In the frog, the tectum receive two retinotopic projections: one from the contralateral eye and one from the ipsilateral eye via the nucleus isthmus These two projections are aligned so the same area of the tectum receive information from both sides of the eye Rotation of one eye disrupt this projection but it is restore over time

39 Synapse Plasticity and Critical Periods Does neuronal plasticity occur during a specific time of neuronal development or can it occur at any point? Somatotopic representation in the cortex is very plastic and depends on the level of use of a particular body part. This plasticity is particularly evident during early periods of development but can occur in the adult brain as well. Disuse or surgical removal of a particular area of the body can result in rearrangement of the somatotopic maps

40 Synapse Plasticity and Critical Periods Does neuronal plasticity occur during a specific time of neuronal development or can it occur at any point? Formation of ocular dominance columns occurs during a specific period of early development (critical period). Monocular deprivation prevents formation of ODC during the first 3 months in the cats life

41 Role of Intersynaptic Interactions Do synaptic interactions regulate synaptic rearrangements in the developing nervous system? Crafting of two motor nerves into the same muscle allows them to maintain contact over several months if axons are crafted far apart Placing the nerves within 1 mm or less, result in the elimination of one set of contacts

42 Role of Intersynaptic Interactions It appears that close contact between two nerves result in synapse elimination. Electrical activity seems to regulate this process. When electrical activity is inhibited, the distance between contacts can be reduced

43 Role of Intersynaptic Interactions Competition between synapses is not the only factor that regulates synaptic rearrangements. Postsynaptic neurons can also regulate synaptic connections In Aplysia,, different dendritic arborizations on the motor neuron receive contact from sensory neurons. In this case only 18% of afferent arbors intermingle, the majority of the afferent arbors remain segregated even when only one afferent neuron is present

44 Disuse Leads to Weak Synapses During development disuse can result in weaker synapses In the cat activity of the inhibitory projection from the medial nucleus of the trapezoid body (MNTB) to the lateral superior olive nucleus (LSO) can be reduced by removing the contralateral ear (denervation)) or treatment with the glycine antagonist strychnine

45 Role of Intersynaptic Interactions Synaptic activity can depress less active inputs The rat lumbrical muscle receives innervation from two separate peripheral nerves LN and SN. Stimulation of SN nerve elicits the strongest contraction in the muscle However, repetitive electrical stimulation of LN results in a weaker contraction of the muscle in response to SN stimulation

46 Heterosynaptic Depression Heterosynaptic interactions due to two competing inputs can induce synaptic destabilization very fast as demonstrated in cultured Xenopus muscle fibers receiving connections from two separate spinal neurons Notice that if one synapse is strongly stimulated for several seconds it has a inhibitory role of the second synapse

47 Role of Intersynaptic Interactions Decreased synaptic strength is a prelude to synapse elimination. Over a period of 8 days in the NMJ, there is a significant reduction in the ability of the weak synapse to generate a PSP whereas the strongest synapse become stronger over similar period In the NMJ, loss of clustered postsynaptic receptors occurs before synaptic elimination

48 Interaction with the Target Increases Intracellular Calcium in the Growth Cone Changes in intracellular calcium concentration are important for synaptic connections Increased intracellular calcium concentration slows down growth cone movement and facilitates synapse formation

49 Interaction with the Target Increases Intracellular Calcium in the Growth Cone Calcium ions play an important role in synaptic elimination. It appears that the fight between synaptic terminals that occurs at the postsynaptic cell requires calcium Depolarizing potentials may open voltage-gated gated Ca 2+ channels and activate Ca 2+ -dependent proteolytic enzymes

50 Role of Calcium Ions in Synaptic Elimination Removal of extracellular calcium ions with the calcium chelator BAPTA result in increased polyneuronal innervation at the NMJ

51 Role of Calcium Ions in Synaptic Elimination Synaptic depression depends on postsynaptic calcium. Increase intracellular calcium depresses synaptic currents M1 no Ca loading M1 Ca loading Whole cell recordings from an innervated myocyte (M2) located near another myocyte filled with a calcium-caged caged compound (M1) Increased calcium concentration in M1, reduced nerve-evoked evoked synaptic currents in M2

52 Role of NMDA Receptors in Synaptic Plasticity In neurons, one main pathway for Ca 2+ influx is activation of NMDA receptors. NMDA receptor are activated by both glutamate and depolarization. At negative membrane potential, NMDA receptors remain close even in the presence of glutamate because extracellular Mg 2+ blockage Membrane depolarization can remove this inhibition

53 Role of NMDA Receptors in Synaptic Plasticity In the three eye mutated frog, the tectum becomes coinnervated by projections from two eyes. These projections are segregated into discreet columns like the ocular dominance columns in the visual cortex Pretreatment with the NMDA antagonist AP-5 5 prevent stripe formation

54 Role of NMDA Receptors in Synaptic Plasticity In mammals, afferent projections from the temporal retina are eliminated from the caudal superior colliculus (SC) NMDA receptor blockade with AP-5 5 prevent removal of caudal projections into the SC

55 Role of camp on Activity-Dependent Synapse Formation In Drosophila, wild type muscle fibers 6 and 7 express Fasciclin II which allow the formation of ~180 boutons In mutant flies (dunce), which express high levels of camp, FascII expression is significantly reduce. Lower FascII expression allows an increase in bouton formation on the muscle

56 Role of camp on Activity-Dependent Synapse Formation In the ether-a-go go-go Shaker flies which show a high level of synaptic activity (due to reduced potassium channel expression) FascII expression is still lower. This result in the formation of a larger number of boutons on the muscle fibers This findings indicate that increased activity result in increased camp in the nerve terminal which decreases FascII expression. This will result in sprouting

57 Role of Electrical Activity on Synapse Formation Electrical activity can also regulate synthesis and release of neurotrophic factors at central synapses. Increased electrical activity increases synthesis of BDNF Increased electrical activity upregulate BDNF synthesis and release in hippocampal neurons. Neurotrophic factors regulate synapse formation and stability in central neurons From Balkowiec & Katz, 2002;

58 Role of Electrical Activity on Synapse Formation Increased electrical activity upregulate BDNF synthesis and release in hippocampal neurons. Neurotrophic factors regulate synapse formation and stability in central neurons From Alcina et la., 2001

59 Activity-Dependent Regulation of the NMJ Motor axons can make contact with slow and fast muscle fibers. Motoneuron innervating fast muscles (i.e., digitorum longus, EDL) can generate only a few thousand impulses per day in brief bursts at high frequency (100 Hz), whereas motoneurons to slow muscles (i.e., soleus, SOL) generate several hundred thousand impulses per day, often in long trains at low frequency (20 Hz) From Reid et al., 2003

60 Activity-Dependent Regulation of the NMJ However, changes in the level of activity of motoneurons can result in significant changes in quantal content and the rate of neurotransmitter release EDL=fast muscle SOL=slow muscle These experiments suggest that fast and slow NMJs display marked plasticity by being able to adapt important release characteristics to the impulse patterns imposed on them From Reid et al., 2003

61 Allosteric Changes in Synaptic Activity Synapses are not only weakened by the activity of neighboring connections. Synapses can become stronger or weak by their own activity In long term potentiation (LTP), tetanic stimulation of a synapse can lead to enhanced response. LTP requires NMDA receptor transmission and is most prominent in the hippocampus and the cortex

62 Allosteric Changes in Synaptic Activity LTP of synaptic activity in the rat barrel cortex is developmentally regulated and occurs during the first postnatal week

63 Changes in Synaptic Function by Intrinsic Activity Intersynaptic interactions are not the only way to modulate synaptic activity Synaptic activity can lead to a decrease in PSP due to long term depression (LTD). In many areas of the brain LTD is predominant during early periods of development In the layer IV of the visual cortex, LTD declines with age

64 Functional vs. Silent Synapse At any given point are all the synapses functional? Silent synapse are nonfunctional synapses that can be turned on by repetitive use. Silent synapse can be detected by comparing the level of anatomical connections with functional recordings From Isaac, 2003 Notice that in synapses undergoing LTP the synaptic potential is already present from the beginning but its amplitude increases by repetitive stimulation

65 Functional vs. Silent Synapse At any given point are all the synapses functional? Silent synapse are nonfunctional synapses that can be turned on by repetitive use. Silent synapse can be detected by comparing the level of anatomical connections with functional recordings NMDA synapses may become silent if they are not depolarized sufficiently to remove Mg 2+ blockade

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